Information

Why are there no complex hermaphrodite land animals?


The title says it all. I know that 'complex' is a pretty ambiguous term to use, but I can't think of a more scientific term/definition for my meaning. I can't think of any large (larger then a small rodent) hermaphrodite species, or any that we tend to think of as having complex structures; hermaphrodite species all seem pretty boring really.

I get why sex is a huge advantage, but by that regard hermaphrodites seem quite powerful. The ability to both produce your own young and impregnate others allow for more young. Plus, it provides the opportunity for a species to choose to self fertilize if no mate is available. I realize sexual reproduction is preferable, by it's nice to have Autogamy as a backup option just in case.

I understand why there are advantages to two sexes, particularly in terms of sexual dimorphism which allows male to be better at potentially reproducing with many females by specializing in it. I completely understand how two genders would evolve and be successful.

What I find odd is that nearly all larger or complex species seem to have genders. I would have thought that, like many other mating strategies, there would be variance across species; with some choosing to be hermaphrodites to increase the maximum children they can produce as a species, by having twice the child bearers, and others choosing to go the sexual dimorphism route by having roles that they are best at. I mean even Obligate parthenogenesis has evolved separately many larger specie like lizards, despite it arguably being an evolutionary dead end in the long term due to the lose of the advantages of sexual reproduction. If adaptations that completely toss away the power of sex evolve all over the place why do new hermaphrodite species never seem to evolve, and existing hermaphrodite species never seem to grow bigger or more diverse?

In particular sequential hermaphrodite, like many aquatic fish use, seems a pretty effective strategy. When your young, and small, play a female role to have guaranteed offspring, only once your big and at your most fit bother competing as a male for access to multiple mates.

A related question, associated with my own attempt to explain why existing hermaphrodite species don't seem to take as many varied forms; but which I'm not really sure I buy. Is it possible that the lack of sexual conflict (primarily, but not limited to, competition between males for mates, driven from the fact that males would have more drive to compete then hermaphrodites since it's their only reproductive strategy), would mean there was less of a drive towards adaptation in hermphrodite species? A sort of red-queen scenario, where your own species is the red queen?


Oxygen triggered the evolution of complex life forms

In the largest study to date that does not focus on vertebrates, researchers from Pennsylvania State University used molecular dating methods to create a new timeline of eukaryotic evolution. By adding information about the numbers of different cell types possessed by each group of organisms, the researchers reconstructed how the complexity of life has increased over time. The study shows that organisms containing more varied cell types evolved following increases in atmospheric oxygen.

Professor Blair Hedges, who led the research team said: "To build a complex multicellular organism, with all the communication and signalling between cells it entails, you need energy. With no oxygen or mitochondria, complex organisms couldn't get enough of this energy to develop."

The study showed that organisms containing more than two or three different cell types appeared soon after the surface environment became oxygenated around 2,300 million years ago. This was around the same time that cells became able to extract the energy from oxygen, thanks to the emergence of mitochondria.

Life forms became even more complex following the evolution of organelles able to produce oxygen. Plastids, such as chloroplasts found in plants, evolved around 1,500 million years ago. During the following 500 million years, organisms that contained up to 50 different cell types evolved. These more complex organisms included algae, which would have benefited directly from being able to produce their own oxygen, and early animals and fungi, which could use this extra oxygen to provide energy for their development.

The authors of the study write: "The results support a deep history for complex multicellular eukaryotes, and implicate oxygen as a possible trigger for the rise in complex life."

To calculate when the different groups of organisms diverged, the researchers compared the sequences of nuclear proteins from a wide range of different organisms using all the available molecular dating methods. All the methods gave similar results.

The pattern and timing of the rise of complex multicellular life during the history of the Earth has not been firmly established. There are large differences between the history suggested by the fossil record, and that estimated using DNA and protein sequence data.

Molecular dating has some obvious advantages over the fossils, however. Hedges said: "This type of information is very difficult to obtain from the fossil record of early life. However the genomes of organisms are packed with millions of bits of data that biologists are now beginning to decipher, and some of those data can be used to tell time."

This press release is based on the following article:

A molecular timescale of eukaryote evolution and the rise of complex multicellular life
Blair Hedges, Jaime E Blair, Venturi Maria and Jason L Shoe
BMC Evolutionary Biology, 2004 4:2
Published 27 January, 2004

When published, this article will be available online free of charge, according to BMC Evolutionary Biology's Open Access policy. View the article at: http://www. biomedcentral. com/ 1471-2148/ 4/ 2/ abstract

For further information about this research please contact Professor Blair Hedges by email at [email protected] or by phone on 814-865-9991

Alternatively, or for further information about the journal or Open Access publishing, please contact Gemma Bradley by email at [email protected] or by phone on 44-207-323-0323.

BMC Evolutionary Biology (http://www. biomedcentral. com/ bmcevolbiol/ ) is published by BioMed Central (http://www. biomedcentral. com), an independent online publishing house committed to providing Open Access to peer-reviewed biological and medical research. This commitment is based on the view that immediate free access to research and the ability to freely archive and reuse published information is essential to the rapid and efficient communication of science. BioMed Central currently publishes over 100 journals across biology and medicine. In addition to open-access original research, BioMed Central also publishes reviews, commentaries and other non-original-research content. Depending on the policies of the individual journal, this content may be open access or provided only to subscribers.

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Introduction

Hermaphroditic plants and animals can potentially maximize reproductive success through a wide variety of different strategies. A key observation for testing sex allocation theory in simultaneous hermaphrodites is the proportion of resources devoted to male vs. female function ( 17 ). The specific allocation strategy followed by a hermaphrodite may affect the extent of sexual selection and mating behaviour ( 44 ). Most models of sex allocation are based on the concept of male and female gain curves (the relationship between relative investment in either male or female gamete production and resulting reproductive success 19 16 , 17 ). These models received substantial empirical support (e.g. in coral reef fishes [ 31 , 32 , 33 34 46 , 47 ], a polychaete worm [ 54 , 55 , 56 ] and in a barnacle [ 49 ]). Most of these hermaphrodites have external fertilization. A variety of hermaphroditic invertebrates, however, have some form of copulation, sperm storage and internal fertilization ( 44 ).

More recently, sex allocation models for outbreeding hermaphrodites with internal fertilization and sperm storage have been developed ( 18 37 ). These models consider how various aspects of sperm competition, such as mating frequency, sperm digestion and different mechanisms of sperm displacement, affect sex allocation in simultaneous hermaphrodites. The models predict that a reduced mating rate leads to a reduction in resources allocated to the male function ( 18 37 ), while sperm digestion leads to an increase in allocation to the male function ( 37 ). At present, there are no data available on relative male/female allocation for internally fertilizing simultaneous hermaphrodites with different mating frequencies.

The research presented here explores sex allocation in Arianta arbustorum, a simultaneous hermaphrodite land snail with internal fertilization, sperm storage and sperm digestion. We designed an experiment to investigate (1) whether snails alter the relative reproductive allocation to the male function with increasing number of copulations, and (2) whether the energy spent on spermatophores and sperm is traded off against energy expended on egg production. For this purpose we examined the number of sperm delivered and eggs produced by snails that mated once, twice or three times within one reproductive season. As measures of resource allocation we assessed the dry mass, nitrogen and carbon content of spermatophores and eggs produced.


Introduction

Sexual selection has come to be seen as a keystone of Charles Darwin's theory of evolution by natural selection, being the exception that proves the rule that evolution proceeds through differential reproduction (see Ghiselin 1969b for discussion). Famously, Darwin developed the theory of sexual selection to account for certain traits such as the weapons used in male-male competition (for example, a stag's antlers) or the ornaments used to attract members of the opposite sex (for example, a peacock's tail) which seemed to be very important in obtaining mates but unimportant otherwise. That these characters were not important in “the struggle for existence” was made clear, he argued, in cases in which the character in question was limited to adult males. In his view, where females and males share the same habitat, food sources, predators, and so on, sexually dimorphic characters must have evolved as a result of differential mating success. Darwin considered sexual selection to be limited to higher animals (from arthropods on up) on two grounds first, “it is almost certain that these animals have too imperfect senses and much too low mental powers to feel mutual rivalry, or to appreciate each other's beauty or other attractions ( Darwin 1871, p 321),” and “In the lowest classes the two sexes are not rarely united in the same individual, and therefore secondary sexual characters cannot be developed” (Darwin 1871, p 321). Darwin, then, saw hermaphroditism as incompatible with sexual selection both because of a lack of opportunity for evolution of sexual dimorphism and a lack of capacity for mate choice and/or direct competition for mates in many invertebrates. Much of sexual selection research still focuses on sexual dimorphism (for example, Shuster and Wade 2003) and sexual dimorphism and secondary sexual characters are often used as proxies for evidence of sexual selection (see Table 1 Shuster and Wade 2003 Jones and others 2004 Kappeler and Van Schaik 2004 Mead and Arnold 2004 see discussion in Andersson 1994) and/or as part of the definition of sexual selection ( Table 1). The first questions to address, then, are the nature of sexual selection and how it might apply to hermaphrodites.

Definitions of sexual selection

(modified from Andersson 1994 Jones and others 2004 Clutton-Brock 2004) .
1. Selection on particular traits arising from intrasexual reproductive competition
2. Selection on particular traits arising from intersexual reproductive competition
3. Mating competition between males
4. Sex differences in traits that confer advantages in competition for mates
5. Variation in male mating success
6. Sex differences in variance in reproductive success (Payne 1979 Wade and Arnold 1980)
7. “Sexual selection is due to variance in reproductive success among members of the same sex and species.” (Gowaty 2004, p 37)
8. Consistent patterns of mate choice by members of either sex
9. Sex differences in the intensity of selection on particular traits
10. Sex differences in the intensity of selection on particular traits caused by contrasting effects of the trait on mating success in the two sexes
11. “Sexual selection is selection that arises from differences in mating success (number of mates that bear or sire progeny over some standardized time interval” (Arnold 1994b, p S9)
12. Selection through competition to acquire mates or be chosen as a mate (Andersson 1994 adopted here)
(modified from Andersson 1994 Jones and others 2004 Clutton-Brock 2004) .
1. Selection on particular traits arising from intrasexual reproductive competition
2. Selection on particular traits arising from intersexual reproductive competition
3. Mating competition between males
4. Sex differences in traits that confer advantages in competition for mates
5. Variation in male mating success
6. Sex differences in variance in reproductive success (Payne 1979 Wade and Arnold 1980)
7. “Sexual selection is due to variance in reproductive success among members of the same sex and species.” (Gowaty 2004, p 37)
8. Consistent patterns of mate choice by members of either sex
9. Sex differences in the intensity of selection on particular traits
10. Sex differences in the intensity of selection on particular traits caused by contrasting effects of the trait on mating success in the two sexes
11. “Sexual selection is selection that arises from differences in mating success (number of mates that bear or sire progeny over some standardized time interval” (Arnold 1994b, p S9)
12. Selection through competition to acquire mates or be chosen as a mate (Andersson 1994 adopted here)

Definitions of sexual selection

(modified from Andersson 1994 Jones and others 2004 Clutton-Brock 2004) .
1. Selection on particular traits arising from intrasexual reproductive competition
2. Selection on particular traits arising from intersexual reproductive competition
3. Mating competition between males
4. Sex differences in traits that confer advantages in competition for mates
5. Variation in male mating success
6. Sex differences in variance in reproductive success (Payne 1979 Wade and Arnold 1980)
7. “Sexual selection is due to variance in reproductive success among members of the same sex and species.” (Gowaty 2004, p 37)
8. Consistent patterns of mate choice by members of either sex
9. Sex differences in the intensity of selection on particular traits
10. Sex differences in the intensity of selection on particular traits caused by contrasting effects of the trait on mating success in the two sexes
11. “Sexual selection is selection that arises from differences in mating success (number of mates that bear or sire progeny over some standardized time interval” (Arnold 1994b, p S9)
12. Selection through competition to acquire mates or be chosen as a mate (Andersson 1994 adopted here)
(modified from Andersson 1994 Jones and others 2004 Clutton-Brock 2004) .
1. Selection on particular traits arising from intrasexual reproductive competition
2. Selection on particular traits arising from intersexual reproductive competition
3. Mating competition between males
4. Sex differences in traits that confer advantages in competition for mates
5. Variation in male mating success
6. Sex differences in variance in reproductive success (Payne 1979 Wade and Arnold 1980)
7. “Sexual selection is due to variance in reproductive success among members of the same sex and species.” (Gowaty 2004, p 37)
8. Consistent patterns of mate choice by members of either sex
9. Sex differences in the intensity of selection on particular traits
10. Sex differences in the intensity of selection on particular traits caused by contrasting effects of the trait on mating success in the two sexes
11. “Sexual selection is selection that arises from differences in mating success (number of mates that bear or sire progeny over some standardized time interval” (Arnold 1994b, p S9)
12. Selection through competition to acquire mates or be chosen as a mate (Andersson 1994 adopted here)

What is sexual selection?

Sexual selection is a term that has meant different things to different people. In a recent review, Tim Clutton-Brock (2004) listed 9 different definitions of sexual selection and the list is not exhaustive (see Table 1). Of those definitions, 4 involve sexual dimorphism (sex differences) and 2 refer only to males. However, the essence of sexual selection as Darwin defined it is selection through competition for mates. Darwin first defined sexual selection early in On the Origin of Species: “what I call Sexual Selection. This depends not on a struggle for existence, but on a struggle between the males for the possession of the females the result is not death to the unsuccessful competitor, but few or no offspring.” ( Darwin 1859, p 88). Fuller treatment of the theory came in The Descent of Man where he defined sexual selection as depending “on the advantage which certain individuals have over the same sex and species, in exclusive relation to reproduction” ( Darwin 1871, p 256). As Andersson (1994) has pointed out, this definition can be applied to all organisms, including plants, since as in ecology, the effect of competition will be the same whether it occurs as interference competition (male-male combat, for example), scramble competition (sperm competition pollen competition), or indirectly such as competition to be chosen by females or by pollinators (see Levitan 1998 Skogsmyr and Lankinen 2002 Delph and Ashman 2006 Thomson 2006). Andersson's (1994) general definition of sexual selection applies to all forms of hermaphrodites as well as taxa, such as protists, that lack anisogamy, making it appropriate to test hypotheses about the origins of sexual selection (contrary to Grant 1995). Therefore, consideration of hermaphrodites shows us the weaknesses of definitions of sexual selection that are specific to sexually dimorphic traits or to males alone. The next questions concern how to identify and measure sexual selection and what its sources may be in hermaphrodites.

Sources of sexual selection

The fundamental question in sexual selection theory has been understanding why it is so often the case that males are “eager,” competing with each other for access to mates, whereas females are “choosy” about whom they mate with. The ultimate explanation for the rule of male-male competition and female choice was seen by Darwin as anisogamy. In surprisingly modern arguments he traced the source of male eagerness and female coyness to (1) the motility of sperm vs. the immobility of eggs and/or (2) the fact that sperm are generally more numerous than eggs. Interestingly, Darwin evoked an energetic argument to explain what he termed “the greater general variability in the male sex” “The female has to expend much organic matter in the formation of her ova, whereas the male expends much force in fierce contests with his rivals, in wandering about in search of the female, in exerting his voice, in pouring out odiferous secretions, &c. … On the whole the expenditure of matter and force in the two sexes is probably nearly equal, though effected in very different ways and at different rates.” ( Darwin 1871, p 219 see also discussion in Ghiselin 1987). Therefore, as is so often the case, in his description and definition of sexual selection, Darwin identified most of the issues that occupy us today. Bateman (1948) hypothesized that males compete for mates and females do not because reproductive success in females is limited by the resources available for egg production, that is, the female gain curve plateaus, whereas the reproductive success of males is limited only by access to females, and the male gain curve is proportional to the number of mates (or eggs) available. This hypothesis has been very influential, but problems with it have begun to be identified (see Hubbell and Johnson 1987 Arnold and Duvall 1994 Gowaty 2004 Leonard 2005 see Tang-Martinez and Ryder 2005 for discussion). The problems identified have been (a) the weakness of Bateman's own data from Drosophila ( Sutherland 1985), (b) evidence that sperm (pollen) can be limiting ( Nakatsuru and Kramer 1982 Willson and Burley 1983 Shapiro and Giraldeau 1996 Levitan 1998) (c) evidence that female choice may not be based on resources (see Gowaty 2004 Gowaty and Hubbell 2005 for discussion) (d) the suggestion that potential reproductive rate and/or breeding sex ratio may better explain the phenomenon (see discussion in Arnold 1994a Arnold and Duvall 1994 Parker and Simmons 1996 Gowaty 2004) (e) evidence from hermaphrodites that females may have higher variance in reproductive success despite larger gametes (see Delph and Ashman 2006), and (f) evidence for a preference for the female role in some hermaphrodites ( Leonard and Lukowiak 1991 Michiels and others 2003 see review in Leonard 2005). Another factor that has been used to explain the pattern of male-male competition and female choice in dieocious animals ( Alexander and Borgia 1979) and the preferred sexual role in simultaneous hermaphrodites ( Leonard and Lukowiak 1984) is the control of fertilization. Alexander and Borgia (1979) argued that a fundamental difference between males and females is that in general, females retain a greater degree of control over the fate of their gametes than do males. The arguments of Bill Eberhard (1996) and Patty Gowaty (2004) suggest that female control of fertilization may represent a form of mate choice. At present, a popular hypothesis is that multiple factors may be at work to set the stage for sexual selection (see Shuster and Wade 2003). Table 2 lists factors that have been considered to be important in determining the strength and direction of sexual selection by producing differences between the sexes (or sexual roles) in variance in reproductive success and consequently skewed breeding sex ratio (BSR). The great difficulty is to determine which differences between the sexes are causes of sexual selection and which are effects. In hermaphrodites each individual acts as both male and female and can act as its own control. Identification of the preferred sexual role in hermaphrodites is one way of testing alternative hypotheses as to the source of sexual conflict (see following sections review in Leonard 2005).

Sources of sexually dimorphic variance in reproductive success

1. Differential per gamete investment (Bateman 1948)
2. Differences in gamete number (Darwin 1871)
3. Differential postzygotic investment (Trivers 1972)
4. Skewed operational sex ratio (Emlen and Oring 1977)
5. Differences in potential mating rate (Baylis 1981 Sutherland 1985 Clutton-Brock and Vincent 1991)
6. Differences in latency between reproductive episodes (Hubbell and Johnson 1987)
7. Skewed breeding sex ratio (Arnold and Duvall 1994)
8. Greater control of fertilization by one sex (Alexander and Borgia 1979 Leonard and Lukowiak 1984)
9. Differential correlation between age/size and fecundity (Size-advantage model Ghiselin 1969a Warner 1975)
10. Differential correlation between age/size and success in competition for mates (Size-advantage model Ghiselin 1969a Warner 1975)
1. Differential per gamete investment (Bateman 1948)
2. Differences in gamete number (Darwin 1871)
3. Differential postzygotic investment (Trivers 1972)
4. Skewed operational sex ratio (Emlen and Oring 1977)
5. Differences in potential mating rate (Baylis 1981 Sutherland 1985 Clutton-Brock and Vincent 1991)
6. Differences in latency between reproductive episodes (Hubbell and Johnson 1987)
7. Skewed breeding sex ratio (Arnold and Duvall 1994)
8. Greater control of fertilization by one sex (Alexander and Borgia 1979 Leonard and Lukowiak 1984)
9. Differential correlation between age/size and fecundity (Size-advantage model Ghiselin 1969a Warner 1975)
10. Differential correlation between age/size and success in competition for mates (Size-advantage model Ghiselin 1969a Warner 1975)

Sources of sexually dimorphic variance in reproductive success

1. Differential per gamete investment (Bateman 1948)
2. Differences in gamete number (Darwin 1871)
3. Differential postzygotic investment (Trivers 1972)
4. Skewed operational sex ratio (Emlen and Oring 1977)
5. Differences in potential mating rate (Baylis 1981 Sutherland 1985 Clutton-Brock and Vincent 1991)
6. Differences in latency between reproductive episodes (Hubbell and Johnson 1987)
7. Skewed breeding sex ratio (Arnold and Duvall 1994)
8. Greater control of fertilization by one sex (Alexander and Borgia 1979 Leonard and Lukowiak 1984)
9. Differential correlation between age/size and fecundity (Size-advantage model Ghiselin 1969a Warner 1975)
10. Differential correlation between age/size and success in competition for mates (Size-advantage model Ghiselin 1969a Warner 1975)
1. Differential per gamete investment (Bateman 1948)
2. Differences in gamete number (Darwin 1871)
3. Differential postzygotic investment (Trivers 1972)
4. Skewed operational sex ratio (Emlen and Oring 1977)
5. Differences in potential mating rate (Baylis 1981 Sutherland 1985 Clutton-Brock and Vincent 1991)
6. Differences in latency between reproductive episodes (Hubbell and Johnson 1987)
7. Skewed breeding sex ratio (Arnold and Duvall 1994)
8. Greater control of fertilization by one sex (Alexander and Borgia 1979 Leonard and Lukowiak 1984)
9. Differential correlation between age/size and fecundity (Size-advantage model Ghiselin 1969a Warner 1975)
10. Differential correlation between age/size and success in competition for mates (Size-advantage model Ghiselin 1969a Warner 1975)

The potential for sexual selection in hermaphrodites

Variance in reproductive success has long been of interest as a measure of sexual selection ( Bateman 1948 Payne 1979 Fincke 1988 Raffetto and others 1990 etc.). The theoretical upper limit to the intensity of selection on a population is given by Crow's Index the ratio of the variance in progeny number to the square of the mean number of progeny ( Crow 1958 Shuster and Wade 2003). The use of Crow's Index as a basis for measuring the intensity of sexual selection ( Wade 1987 Shuster and Wade 2003) is an important development in sexual selection theory but the current usage, Imates ( Shuster and Wade 2003), is inappropriate for hermaphroditic taxa because it focuses on male mating success as a fraction of the total. With separate sexes, in each generation sexual selection acting on males will be separate from that acting on females. In either sequential or simultaneous hermaphrodites however, sexual selection on an individual comes from the total of its success in both sexual roles. An appropriate measure of sexual selection for hermaphrodites would therefore have to include variance in total reproductive success. Clearly, the intensity of sexual selection cannot be larger than total selection so that Crow's Index represents a theoretical upper limit to the strength of sexual selection. In reality, sexual selection will seldom or never reach this upper limit since other forces of selection are expected to be in operation, although it might be possible to construct experimental conditions that would bring a population close. Also, it should be emphasized that the magnitude of the variance is a measure of the potential for selection and not a measure of the intensity of selection (see discussion Wade 1987 Grafen 1987) random factors could also produce variance in reproductive success (see Sutherland 1985, 1987). However, differences in variance in reproductive success among populations with similar life histories and biology, would offer a first approximation to the potential for sexual selection.


SEXUAL CONFLICTS IN SIMULTANEOUS HERMAPHRODITES

Simultaneous Hermaphrodites: The Basics

Simultaneous hermaphroditism could be favored (1) by facilitating reproductive assurance when individuals (or their gametes) risk failed reproduction for lack of encountering partners (Darwin 1876 Tomlinson 1966 Ghiselin 1969), (2) if the male and female reproductive functions do not (strongly) trade off, because they have nonoverlapping resource requirements or can share costs (Charnov et al. 1976 Heath 1979), or (3) if the investment to a sex function shows diminishing fitness returns (e.g., because of low mobility) (Ghiselin 1969), restricted “mating group size” (Charnov 1980), and/or local sperm competition (Schärer 2009 Schärer and Pen 2013), thus favoring reallocation of remaining reproductive resources to the other sex function. The balance of evidence suggests that all these factors may play some role, but the last is likely the most important, at least in animals (reviewed in Schärer 2009).

The best-studied determinant of sex allocation in simultaneous hermaphrodites is the mating group size, which affects the strength of male–male competition in a local group. If mating group size is very small, then little is gained from male investment beyond some minimum needed to ensure full fertility because sperm from a single ejaculate largely compete among themselves for fertilization (termed “local sperm competition” in Schärer 2009) and more is gained from reallocating resources to the female function, resulting in a stable female-biased sex allocation. As mating group size increases, however, success in sperm competition (between sperm from different donors) (Parker 1970) becomes increasingly important to determining fitness through the male sex function, favoring a greater male investment and thus a more even sex allocation. Of course, mating group size can vary in space and time, which in many species has favored the ability to plastically adjust sex allocation to the prevailing (social) conditions (reviewed in Schärer 2009). Such sex allocation adjustment mechanisms could potentially be manipulated by mating partners and are therefore a putative target of sexual conflict in simultaneous hermaphrodites (Charnov 1979 Michiels 1998 Schärer 2009 Schärer and Janicke 2009 see also below).

Intralocus Sexual Conflict

Most work on simultaneous hermaphrodites concerns interlocus sexual conflict (see below), and with respect to intralocus sexual conflict, there are many parallels with sequential hermaphrodites, so this section will be brief. In simultaneous hermaphrodites, male and female fitness is probably also often distributed differently over individuals in a population, and although individuals generally exhibit both sex functions simultaneously, the emphasis often shifts with size (or age), leading to size-dependent sex allocation (Klinkhamer and de Jong 1997 Schärer et al. 2001 Schärer 2009). So here again we can expect linkage to arise between sexually antagonistic alleles and alleles that influence sex allocation (and note here that the latter can again be viewed as largely equivalent to the former). Although there is now ample evidence that sex allocation can be extremely plastic in many simultaneous hermaphrodites (Schärer 2009), there is also some evidence for standing genetic variation in sex allocation (e.g., Hughes 1989 Yund et al. 1997 S Ramm and L Schärer, unpubl.), thus such linkage is clearly possible. Moreover, many traits in simultaneous hermaphrodites may evolve as a result of interlocus sexual conflict and antagonistic coevolution (see below), so there could be many sexually antagonistic alleles with asymmetric fitness effects. For example, a novel seminal fluid (male persistence) allele could have a weak negative (pleiotropic) effect on the female function of its carrier (e.g., because of general toxicity or negative effects during selfing), which is to say that an allele that arises in the context of interlocus sexual conflict (aimed at manipulating the mating partner) can simultaneously generate intralocus sexual conflict (by imposing harm on the carrier's own female function). Similar effects could result from any allele involved in sexually antagonistic coevolution, and most if not all such alleles likely involve some degree of intralocus sexual conflict, if only because investment in the relevant trait draws resources from a common resource pool (and thus likely comes at some cost to the individual, including its female sex function). In the remaining subsections, we focus on different aspects of interlocus sexual conflict.

Premating Conflicts: The Battleground

Sexual conflicts over mating (“mating conflicts”) in simultaneous hermaphrodites relate to asymmetries between acting as a sperm donor or sperm recipient in the benefits of mating versus its costs (Table 1) and manifest themselves in unique conflicts over mating interactions (Charnov 1979 Michiels 1998). The evolutionary battleground for such mating conflicts can be visualized as a matrix of compatible and incompatible behavioral interactions, which are defined by the interest of two individuals to be a sperm donor, a sperm recipient, or both (Fig. 2A) (Michiels 1998). Mating conflicts occur whenever the interacting individuals want to adopt incompatible sex roles. We first review the theoretical framework and empirical evidence for sex-role preferences, as they represent a key assumption for mating conflicts to arise, and then discuss hypotheses developed for, and evidence bearing on, the resolution of such conflicts.

Evolutionary battleground of mating conflicts in simultaneous hermaphrodites (modified from Michiels 1998) and some potential routes to resolution. (A) Mating conflicts between individuals A and B can arise from incompatible interests to donate and/or receive sperm. (B–G) The routes to resolution of mating conflicts over incompatible interests (i.e., donate sperm, d receive sperm, r or both donate and receive sperm, d&r) encompass the following possibilities (viewed from individual A's perspective): forced unilateral insemination (B) gamete trading with alternating unilateral matings, namely, egg trading (C) or sperm trading (D) by-product reciprocity (E) and gamete trading during reciprocal matings, namely, conditional sperm receipt (F) or conditional sperm donation (G). Red squares in A and the circles in B–G characterize the conflict over mating. Dashed arrows indicate the optimal behavioral outcome for individual A and solid arrows denote the realized behavioral outcome for a given resolution of mating conflict. Yellow squares in B–G point to the type of interaction by which the conflict is resolved reflecting benefits (black circles) and costs (open circles) for individual A. Note that by-product reciprocity (E) does not actually involve conflict (no yellow squares), but it looks superficially similar to cases that do and so is included here for comparison. Specifically, the curved arrows connecting the upper-right and bottom-left squares in E are similar to the cases of alternating unilateral matings in C and D, and the central squares in E are similar to the cases of reciprocal matings in F and G.

Premating Conflicts: Sex-Role Preferences

The theoretical foundations of sex-role preferences date back to Bateman (1948), who compared the fitness benefits of mating between male and female fruit flies. The study revealed a “greater dependence of males for their fertility on frequency of insemination” (Fig. 3) (later coined “Bateman's principle” by Charnov 1979) and suggested this pattern is “an almost universal attribute of sexual reproduction” in both animals and plants (Bateman 1948), thus presumably including hermaphrodites. Three decades later, Charnov (1979) explored the hypothesis that Bateman’s principle also applies to simultaneous hermaphrodites, arguing that hermaphroditic individuals may “copulate not so much to gain sperm to fertilize eggs as to give sperm away,” which he expected to result in an overall preference for the male role and frequent conflicts of interest between mating partners (Fig. 2A, upper-left panel of the matrix).

Schematic illustration of Bateman’s three principles as proposed by Arnold (1994). The sex that experiences the stronger sexual selection (usually the male or sperm donor) is predicted to show (1) a higher relativized variance in reproductive success (also called opportunity for selection, I), (2) a higher relativized variance in mating success (also called opportunity for sexual selection, Is), and (3) a steeper Bateman gradient (i.e., the slope of an ordinary least squares regression of reproductive success on mating success also called sexual selection gradient, β Arnold and Duvall 1994). The graph shows arbitrary data for the male (m gray circles and density curves solid line) and female (f open circles and density curves dashed line) sex. Note that in simultaneous hermaphrodites, the male and female estimates can be obtained from the same individual, so that reproductive success of one sex function can be regressed on mating success of the other sex function. The slopes of such regressions denote “cross-sex effects” that are indicative of trade-offs in sex allocation or sexual antagonism. (Adapted from Anthes et al. 2010.)

Empirical data in terms of so-called Bateman gradients (Fig. 3) are still limited, but they tend to support Charnov’s contention. In the freshwater gastropods, Biomphalaria glabrata and Physa acuta, the male gradients are steeper than the female gradients (Anthes et al. 2010 Pélissié et al. 2012). It is important to spell out why this may often be the case, particularly in species with internal fertilization and sperm storage. The shallow female gradient mainly results from what happens after the first mating in the female role, at which point the female function may have sufficient stored sperm to maintain fertility (i.e., a single mating can potentially switch the female function from infertile to fully fertile). So if one counts the number of “profitable” matings that can be achieved through the male and female function, there are clearly more to be had through the male function (i.e., the male function may obtain some fitness each time the individual mates as a male). The overall male sex-role preference could then simply be seen as a sampling effect. A randomly sampled individual in the population will normally gain more from mating next as a male, because it likely has mated as a female already. The empirically observed Bateman gradients thus probably mean that these snails show a male sex-role preference (Anthes et al. 2010 Pélissié et al. 2012), and two studies on sea slugs, in which only the female function was examined, even suggested costs for high female mating rates (Sprenger et al. 2008 Lange et al. 2012).

This perspective suggests that sex-role preferences need not be fixed, as emphasized by the “gender-ratio hypothesis” (Anthes et al. 2006b). Even if one sex function can usually benefit more from an additional mating, the actual fitness gains from mating as a male or female during any particular encounter will depend on a range of factors, notably the mating history (and thus sperm reserves as both donor and recipient) (e.g., Wethington and Dillon 1996 Anthes et al. 2006a Ludwig and Walsh 2008), as well as other life-history traits, such as fecundity, survival, and sex allocation of the sperm donor and/or the recipient (e.g., DeWitt 1996 Gianguzza et al. 2004 Janicke and Schärer 2009b Dillen et al. 2010). This provides a more flexible framework for thinking about variation in sex-role preferences (Anthes et al. 2006b), and all that is required for conflict is that at least some encounters lead to incompatible mating interests.

Measuring male and female Bateman gradients is clearly a promising approach to predict sex-role preferences and the intensity of the resulting mating conflicts (expressed as the slope difference) (see also Anthes et al. 2010). However, Bateman gradients only quantify the average fitness returns an individual can expect from an additional mating in a given sex role, whereas they ignore the costs that have accrued to obtain that fitness (Jennions and Kokko 2010 Kokko et al. 2012). These costs might also be affected as a result of sex allocation biases (Schärer 2009). Specifically, a female-biased sex allocation will, given the Fisher condition, on average lead to a higher fitness return per unit resource investment to the male sex function. Investing one unit of resource into mating in the male role could therefore potentially be more profitable than investing the same amount in the female role. Given that a female-biased sex allocation is predicted under many conditions and actually observed in many species (reviewed in Schärer 2009 Schärer and Pen 2013), this could potentially further contribute to a preference for the male sex role among simultaneous hermaphrodites.

Alternative ideas about sex-role preferences instead predict a female preference. For example, many simultaneous hermaphrodites possess specific organs to digest sperm and/or other ejaculate components (reviewed in Baur 1998 Michiels 1998 Nakadera and Koene 2013) and so direct (nongenetic) benefits from mating in the female role could potentially result from ejaculate digestion, which might generate a female sex-role preference. However, to our knowledge, evidence that the digestion of ejaculates is actually energetically beneficial to the recipient is still lacking (see Postmating Conflicts sections below). Other direct benefits of multiple mating, such as nuptial gifts or paternal care, are presumably also of minor importance as the former, to our knowledge, do not exist (other than possibly via ejaculates see below) and the latter is rare in simultaneous hermaphrodites (but see Sella and Ramella 1999).

An additional hypothesis posits that a critical factor for sex-role preferences is the risk of one’s gametes remaining unfertilized. Specifically, the “gamete trading hypothesis” (Leonard and Lukowiak 1984, 1985 Leonard 1990) assumes that (1) in internally fertilizing hermaphrodites, it is the female role that has more control over the fate of the invested gametes and that this role may therefore be preferred (although there is accumulating evidence that sperm donors often retain at least some control over the fate of their gametes see also the Postmating Conflicts sections below). Moreover, the hypothesis assumes that (2) in externally fertilizing species, the male role should be preferred as eggs are often released before sperm, which carries the risk they will not be fertilized. However, this implies that a sperm donor would decline to fertilize, at presumably small cost, the (costly) eggs spawned by the partner, even after having invested in precopulatory interactions, which seems implausible (and would probably have to be seen as spiteful behavior). And finally, the gamete trading hypothesis is based on the assumption that the low-risk strategy has a higher mean fitness, which cannot hold given the Fisher condition, as previously pointed out by Greeff and Michiels (1999).

Overall, the currently available empirical evidence suggests a preference to copulate in the male sex role to be generally more likely, but the conditions thought to favor a female sex-role preference remain largely unexplored. Continued efforts to measure the strength of sexual selection in a range of different hermaphroditic systems (Lorenzi and Sella 2008 Anthes et al. 2010 Pélissié et al. 2012) will likely permit a better understanding of Bateman’s three principles (Fig. 3) and enable these and some additional proposed hypotheses for sex-role preferences to be properly evaluated (e.g., Crowley et al. 1998 Leonard 1999 reviewed in Leonard 2005, 2006).

Premating Conflicts: Routes to Resolution

Mating conflicts in simultaneous hermaphrodites appear to be resolved in various ways, ranging from the selfish imposition of the nonpreferred role on the mating partner to putatively cooperative mating interactions (Fig. 2B–G). A common approach to predict behavioral strategies arising from conflicts over preferred sex roles is game theory. For example, Axelrod and Hamilton (1981) used an iterated Prisoner’s Dilemma to model the intriguing mating behavior of a reef fish, the black hamlet Hypoplectrus nigricans—first observed and termed “egg trading” by Fischer (1980)—and they suggested that it involves conditional reciprocity via a tit-for-tat strategy, thus potentially resolving mating conflicts arising from a shared interest to donate sperm in a cooperative way (see also Fischer 1988 Leonard 1990 Crowley et al. 1998). However, we discuss egg trading in some detail below and conclude that the payoff matrices of these models probably do not properly capture the biology of the black hamlet. This example clearly illustrates the need for empirical data that enable the possible strategies to be properly defined and thereby parameterize the payoff matrix of a given mating interaction to predict how mating conflicts could be resolved. This requires not just extensive knowledge about the reproductive biology of a given system, but also about how environmental conditions (such as density and predation risk) may alter the payoffs for reciprocation and defection (Crowley and Hart 2007 Hart et al. 2010). Ultimately, one probably needs manipulative experiments to assess the costs and benefits of the different strategies, to corroborate the importance of particular traits and mating states, and to substantiate claims of strategies involving conditionality (see, e.g., Anthes et al. 2005).

To illustrate the great diversity of behavioral adaptations putatively arising from mating conflicts we start with an apparently simple form of conflict resolution—forced unilateral insemination (Fig. 2B)—which seems to be associated with high costs of sperm receipt, making cooperative behaviors presumably unlikely to evolve. Such overt conflict characterizes the mating behavior of the marine polyclad flatworm Pseudoceros bifurcus, in which both interacting individuals attempt to inject sperm hypodermically into their opponent, while trying to avoid being stabbed themselves, as the latter incurs costs of injury (Michiels and Newman 1998 Arnqvist and Rowe 2005). This so-called “penis-fencing” supposedly originates from a higher benefit of sperm donation, although experimental evidence for a male preference to copulate is also still lacking for this species (for other examples of forced unilateral matings, see Michiels 1998, and references therein).

Unilateral matings may also occur consensually when the mating interests of both partners are compatible. For example, many freshwater gastropods mate unilaterally without it resembling the hit-and-run strategy outlined before for flatworms. In such systems, the mating status and thus the amount of available allosperm (i.e., received sperm to fertilize own eggs) and autosperm (i.e., produced sperm and/or seminal fluid for donation) might predict a preference for playing the male or female role at any one time (Wethington and Dillon 1996 Koene and ter Maat 2005), even in the presence of an overall sex-role preference (see “gender-ratio hypothesis” above) (Anthes et al. 2006b). In these systems, occasional conflicts arising from a shared male preference might simply be resolved by an evasive behavior of the would-be female-acting snail (DeWitt 1991 Wethington and Dillon 1996).

Several unilaterally copulating simultaneous hermaphrodites exhibit pronounced sex-role alternation when mating, which is considered one of the best examples for cooperative behavior via reciprocity (Dugatkin 1997). However, for many of the studied systems it remains unclear whether the observed alternation of sex roles actually involves conditionality (i.e., actual trading of eggs or sperm see Fig. 2C and 2D, respectively), or whether it is just a side effect of a mutual willingness (1) to copulate in both sex roles, or (2) to copulate in one sex role while not objecting to mating in the other (herein called “by-product reciprocity,” curved arrows connecting the upper-right and bottom-left panels in Fig. 2E) (Michiels 1998 Anthes and Michiels 2005 Facon et al. 2008).

As briefly outlined above, alternating unilateral exchange of gametes was first described by Fischer (1980), who, based on behavioral observations, suggested that in the black hamlet (and some other serranid reef fishes), a conflict over mating in the male role is resolved by “egg trading.” Egg trading involves the parceling of the clutch into small subunits, which are then conditionally exchanged by alternating between adopting the preferred sex role, sperm donation, and the nonpreferred sex role, egg donation (or sperm receipt) (Fig. 2C) (Fischer 1980, 1984, 1987 Pressley 1981 Petersen 1995, 2006). Early approaches modeled this as a two-player game with no option to desert and mate with another individual (Axelrod and Hamilton 1981 Fischer 1988 Leonard 1990). However, Connor (1992) showed that incorporating costs of desertion (e.g., for mate searching or higher predation risk) and allowing the size of the egg parcels to be adjusted may in fact make it more profitable to offer the next batch of eggs to the current partner than to leave in search of other mating opportunities. Moreover, Petersen (2006) stressed that the model assumption of equivalent players and symmetric payoffs are often violated and that we therefore urgently need field estimates of parcel size in egg-trading fish. Similarly, egg trading has been proposed to occur during mating interactions of externally fertilizing polychaetes of the genus Ophryotrocha, which also show serial alternation of sex roles (Sella 1985, 1988 Sella et al. 1997 Sella and Lorenzi 2000). However, for both of these putative egg-trading systems, firm experimental corroboration of conditionality (e.g., by showing punishment of experimental cheaters) is still lacking and an overall preference for mating in the male sex function has, so far, only been assumed rather than tested.

Another form of alternating unilateral exchange of gametes, sperm trading (Fig. 2D), was suggested to occur in sea slugs (Leonard and Lukowiak 1984, 1991 Karlsson and Haase 2002 Michiels et al. 2003 Anthes et al. 2005 but see Anthes and Michiels 2005). However, in most of these empirical studies, sperm trading was only inferred from the alternating unilateral exchange of sperm, which might in theory also arise as a by-product of a shared preference to donate with no objection to receive sperm (see Fig. 2E) (Michiels 1998 Puurtinen and Kaitala 2002 Schärer and Pen 2013). Convincing support for conditional sperm trading comes from just a single study. Anthes et al. (2005) experimentally manipulated the ability to donate sperm in the sea slug Chelidonura hirundinina, showing that individuals are reluctant to continue mating with such a nonreciprocating partner. Nevertheless, this observed reluctance could still be interpreted as a rejection of nonpreferred mating partners, rather than a punishment of cheaters, if sperm donation serves as a sexual signal indicating the viability of the donor, as hypothesized by Landolfa (2002).

Initially, sperm trading was proposed to occur in internally fertilizing hermaphrodites with an overall preference to copulate in the female sex function based on the “gamete-trading hypothesis” (see previous subsection Leonard and Lukowiak 1984). In contrast, it has also been argued that sperm trading can be associated with a male sex-role preference even if ejaculates are costly for the donor and provide an energetic benefit to the receiver (Greeff and Michiels 1999). According to this so-called “opportunistic male hypothesis” sperm donors trade their nutrient-rich ejaculates to get access to the eggs of their opponents (Michiels et al. 2003). Here, the ejaculate may function as a nuptial gift and potentially as paternal investment in addition to its usual function in mediating sperm donation to fertilize eggs (Yamaguchi et al. 2012), as has been proposed for many gonochorists (e.g., Vahed 1998). We, however, see problems with this nuptial gift argument, namely, that there must be a considerable energy conversion loss when sperm is first produced and then digested (see also Leonard 2005) and that (just as with nuptial gifts in general) there is no guarantee that the partner will actually use the received energy to make eggs (or that the already existing eggs would preferentially be fertilized by that donor). Both these caveats mean that fitness could usually be obtained much more reliably by instead investing the resources into the own female function. Indeed, when considering a commonly observed energy transfer efficiency between trophic levels of 10% (Pauly and Christensen 1995), rather than the probably unrealistically high value of 50% used by Yamaguchi et al. (2012), then the increase in male allocation compared to their model without a nuptial gift effect is indeed minute (<1%–2% in most cases). And finally, the opportunistic male hypothesis relies on the thus far unproven assumption that sperm digestion actually yields a net resource benefit to the sperm recipient (see the Postmating Conflicts sections below).

Finally, many simultaneous hermaphrodites such as flatworms, annelids, and gastropods show reciprocal mating by donating and receiving sperm at the same time (e.g., Vreys and Michiels 1997 Baur et al. 1998 Michiels and Streng 1998 Michiels and Bakovski 2000 Schärer et al. 2004 Jordaens et al. 2005 Domínguez and Velando 2013), which may or may not result from a conflict over the preferred sex role (see also Puurtinen and Kaitala 2002). In practice, it will usually be difficult to distinguish conditional sperm receipt (Fig. 2F) and conditional sperm donation (Fig. 2G) from by-product reciprocity (Fig. 2E) in reciprocally mating hermaphrodites (Anthes and Michiels 2005), unless sperm transfer can be measured and experimentally manipulated simultaneously in a given copulation, clearly a very challenging task.

To conclude, mating conflicts in simultaneous hermaphrodites are apparently resolved in ways which seem to reflect, at least partially, the proposed asymmetries in the net benefit of acting as a sperm donor and recipient. However, even for well-studied systems we usually still lack detailed information on the payoffs of the observed behavioral strategies, which are needed to fully understand how the mating conflict is resolved. Consequently, it is too early to speculate on the relative incidence of the different types of conflict resolution.

Postmating Conflicts: The Battleground

Even after mating, there remains scope for conflicts of interest between the sperm donor and sperm recipient. Many of these are similar to the phenomena occurring between males and females in gonochorists. Often, however, we expect postmating conflicts to be especially relevant in simultaneous hermaphrodites, for two main reasons: (1) because of the apparent scarcity of overt premating sexually selected traits and the frequent willingness of both partners to mate (or their inability to avoid doing so), meaning we can expect a general shift in sexual selection from the pre- to the postmating arena, and (2) because simultaneous hermaphroditism creates unique targets for sexual conflict, most notably via manipulating also the male sex function and overall sex allocation of the mating partner (Charnov 1979 Michiels 1998 Arnqvist and Rowe 2005 Schärer 2009 Schärer and Janicke 2009). Below, we examine postmating conflicts first from the perspective of the sperm donor attempting to manipulate the sperm recipient and then from the perspective of the sperm recipient attempting to retain or regain control of events occurring after mating.

Postmating Conflicts: Interests of the Sperm Donor

Just as for males in gonochorists (see Edward et al. 2014), several adaptations in simultaneous hermaphrodites likely function to maximize the fertilization success of sperm donors under sperm competition, in a manner that may not be in the recipient’s interest. Relevant traits include the number (e.g., Velando et al. 2008) and morphology (e.g., Schärer et al. 2011) of sperm transferred mechanisms for the efficient transfer of sperm (e.g., Janicke and Schärer 2009a), or for physical displacement of previously deposited sperm (a proposed function of the “disposable” penis of the sea slug Chromodoris reticulata, Sekizawa et al. 2013) suppression of remating by sperm recipients (see below) and maximization of the amount of transferred sperm that are retained in storage and used for fertilization (e.g., Landolfa et al. 2001 Rogers and Chase 2002 Chase and Blanchard 2006 Dillen et al. 2009 Garefalaki et al. 2010 Kimura and Chiba 2013). In the following, we discuss first one especially relevant target of manipulation in simultaneous hermaphrodites, namely, aspects of the recipient’s sex allocation (Charnov 1979 Michiels 1998), and then consider the various ways in which manipulative substances can be transferred from the donor to the recipient.

Two main types of sex allocation manipulation can be envisaged (Schärer 2009, 2014 Schärer and Janicke 2009). First, the sperm donor could directly affect the female function of the sperm recipient in whatever manner maximizes its reproductive success, and this is essentially analogous to a male manipulating a female in gonochorists. Alternatively, the sperm donor could indirectly boost the mating partner’s female function by attacking that individual’s male function, assuming that this actually leads to a reallocation of resources to the recipient’s female sex function (i.e., assuming plasticity and a sex allocation trade-off), and further assuming that the sperm donor itself gains some advantage from this relative to its competitors, which cannot just be assumed (Schärer 2014). Manipulating the partner’s sex allocation should therefore be particularly advantageous in species with low levels of multiple mating, in which manipulation would likely yield benefits exclusively or mainly to the manipulating individual. In this context, a second potential advantage of attacking the recipient’s male function may also be to boost the donor’s paternity share, as an impeded male function may prevent the recipient from remating in either sex role, which might lower the level of sperm competition experienced by the manipulating focal (see Schärer 2014).

A major route through which manipulative substances (collectively termed “allohormones”) (Koene and Chase 1998 Koene and ter Maat 2001) can be transferred from donor to the recipient is in the ejaculate (Zizzari et al. 2014). Seminal-fluid-mediated effects are increasingly recognized as a common source of sexual conflict (see Sirot et al. 2014), also in simultaneous hermaphrodites, as originally predicted by Charnov (1979). For example, seminal fluid investment (as indicated by variation in prostate gland size) covaries with female reproductive tract morphology among opisthobranch sea slugs in a manner consistent with sexually antagonistic coevolution (Anthes et al. 2008). Moreover, the receipt of possibly manipulative seminal fluid substances could explain why Macrostomum lignano flatworms mated to virgin partners (that have more seminal fluid in storage to transfer) are less likely to perform the postcopulatory “suck” behavior, hypothesized to function in influencing the fate of received ejaculate components (Marie-Orleach et al. 2013).

By far the best-studied hermaphroditic system with respect to seminal fluid function is the pond snail Lymnaea stagnalis, in which several seminal fluid components have recently been identified that influence the partner's reproductive behavior and/or resource allocation. One protein called LyAcp10 (also called ovipostatin) suppresses short-term egg production (Koene et al. 2010), by reducing the number of eggs produced (see also Van Duivenboden et al. 1985 Koene et al. 2006, 2009), while apparently increasing the biomass associated with each egg (Hoffer et al. 2012), although precisely what advantage the sperm donor may gain from this remains unclear. Moreover, an intriguing study by Nakadera et al. (2014) recently found an even more surprising effect, namely, that two proteins (LyAcp5 and LyAcp8b) significantly decrease the amount of sperm a recipient transfers in its next mating (note that LyAcp10 may actually have a similar effect). These studies are clearly highly relevant in the context of the sex allocation manipulations discussed above, but given that they focused on measuring short-term effects on female and male reproduction, respectively, it is currently difficult to interpret these findings. Future studies should aim at simultaneously measuring effects on both sexes, preferably over longer time periods (Schärer 2014).

A second route through which manipulative substances can be transferred from sperm donor to recipient, and one that appears especially common in simultaneous hermaphrodites (Lange et al. 2013a), is via accessory structures that appear to have evolved specifically for this purpose (Zizzari et al. 2014). Striking adaptations in this context are the so-called “love darts” of various land snails (reviewed in Koene 2006 Chase 2007). Experimental evidence in Cornu aspersum (formerly Helix aspersa) indicates that these sharp, calcareous structures—injected into the mating partner's body before copulation—transfer bioactive substances that cause muscular contractions of the female reproductive tract (Koene and Chase 1998), promoting sperm storage (Rogers and Chase 2001), and enhancing paternity success (Landolfa et al. 2001 Rogers and Chase 2002 Chase and Blanchard 2006). In contrast, the mucus transferred via the love dart of the snail Euhadra quaesita appears to suppress remating in recipient individuals (Kimura et al. 2013), suggesting that dart shooting can serve multiple functions (see also Adamo and Chase 1990). Love darts may be counter to sperm recipient’s interests for two reasons: by (1) wounding them (Baur 1998, but see Chase and Vaga 2006), and (2) manipulating their reproductive physiology or behavior. As might then be expected from the resulting interlocus sexual conflicts, love darts are highly variable across species (Koene and Schulenburg 2005 Koene et al. 2013) and display signatures of antagonistic coevolution and counteradaptation by sperm recipients in the form of modified reproductive organ morphologies (Koene and Schulenburg 2005 see also Davison et al. 2005 Beese et al. 2009 Sauer and Hausdorf 2009). Similar functions may be performed by the copulatory setae of earthworms (Koene et al. 2002, 2005 König et al. 2006) and devices such as the stylet-like penis appendage found in Siphopteron sea slugs (Anthes and Michiels 2007 Lange et al. 2014) and the penial gland that is everted following external sperm exchange in Deroceras land slugs (Reise 2007 Reise et al. 2007 Benke et al. 2010 for a recent review of “traumatic secretion transfer,” see also Beese et al. 2009 and Lange et al. 2013a). In all of these cases, however, the exact costs and benefits to donor and recipient because of either wounding or receipt of a specific (manipulative) substance under naturalistic conditions remain to be determined.

Irrespective of their method of delivery, allohormones in simultaneous hermaphrodites have been predicted to differ from those in gonochorists. In the former, both male and female substances are expressed in all individuals, which might permit donors to more easily “borrow” their own female substances to manipulate their mating partners, whereas in the latter, such substances will usually have sex-specific expression, which might require more drastic changes in expression (Koene 2005). Too few allohormones have so far been identified to permit a meaningful comparison between sexual systems, but even in hermaphrodites such female substances are normally expressed at different levels in different tissues and would still presumably need to be expressed more highly in novel tissues before they could be coopted by the male function. So the differences between sexual systems may not be so profound in this respect.

Postmating Conflicts: Interests of the Sperm Recipient

As we have seen, individual simultaneous hermaphrodites may often either agree to mate reciprocally or be unable to avoid mating in the role of sperm recipient. This means that they will typically receive many ejaculates. Receiving large amounts of sperm and/or other ejaculate components could be problematic for several reasons, some of which can be seen as either (1) naturally selected (e.g., owing to an increased risk of polyspermy, an increased exposure to sexually transmitted pathogens, and the need to remove a large amount of foreign material from the site of ejaculate receipt), (2) driven by antagonistic coevolution (e.g., avoiding ejaculate-mediated manipulation by the sperm donor), or (3) by sexual selection (e.g., choosing sperm of specific donors). There is thus likely to be a strong incentive for the sperm recipients to control the fate of received substances, and one possible solution is to evolve means of sperm (ejaculate) digestion. There can be no doubt that significant sperm digestion occurs, with well-developed sperm-digesting organs described for example in gastropods (Beeman 1970 Brandriff and Beeman 1973 Beeman 1977 Beese et al. 2006), flatworms (Sluys 1989), and oligochaetes (Westheide 1999). Similarly, even in species with traumatic insemination (see below) that lack specific sperm receiving organs, received sperm appear to be rapidly cleared from recipients (e.g., Macrostomum hystrix S Ramm, A Schlatter, M Poirier, and L Schärer, unpubl.). Although we expect a net fitness benefit to sperm digestion (otherwise it could not have evolved), what is less clear to date is whether sperm recipients can actually recoup any net nutritional benefit from sperm digestion (it could, at least initially, also occur at a net energetic cost). This is an important empirical question, because some recent arguments for mating conflict resolution based on sperm trading assume such a nutritional benefit (“opportunistic male hypothesis”) (Greeff and Michiels 1999 Michiels et al. 2003 see also Yamaguchi et al. 2012).

Any hurdle to fertilization that the sperm recipient erects (i.e., any resistance trait, sensu Rowe et al. 2005) is expected to lead to counterselection on sperm donors to overcome these defenses and is likely to lead to paternity being biased toward particular (persistent) sperm donors (leading to cryptic female choice, sensu Pitnick and Brown 2000). A number of potential mechanisms for cryptic female choice have been proposed. These include the differential storage and usage of sperm from multiple sperm storage tubules (Baur 2007 but see Koemtzopoulos and Staikou 2007), the postmating “suck” behavior of M. lignano already mentioned above (Schärer et al. 2004 Vizoso et al. 2010 Marie-Orleach et al. 2013), and the blocking and phagocytosis of received self-sperm and certain allosperm in the oviduct, and thus preferential fertilization by allosperm from “preferred” clones in the spermcasting ascidian Diplosoma listerianum (Bishop 1996 Bishop et al. 1996 Pemberton et al. 2004). Sperm recipients may also retain more control of sperm uptake, and hence paternity outcomes, when transfer occurs via the external exchange of spermatophores (e.g., in the nudibranch Aeolidiella glauca) (Haase and Karlsson 2000 Karlsson and Haase 2002 see also Bishop and Pemberton 2006). Again, though, it is not clear in all of these cases whether or precisely how the sperm recipient gains direct or indirect fitness benefits from exerting control.

Finally, should sperm recipients gain considerable control over received ejaculates, this could, as originally predicted by Charnov (1979), set the stage for sperm donors to attempt to bypass the ordinary route to fertilization and instead transfer sperm via traumatic insemination into some other part of the recipient’s body (e.g., Angeloni 2003 Anthes and Michiels 2007 Schmitt et al. 2007 Smolensky et al. 2009 Schärer et al. 2011 Lange et al. 2012, 2013b see also Premating Conflicts sections above). Wounding during insemination, and the subsequent need to process/remove ejaculate components transferred in this manner, likely results in significant costs of traumatic insemination to the sperm recipient (e.g., Smolensky et al. 2009 see also Reinhardt et al. 2014). The taxonomic distribution of traumatic insemination suggests that the evolution of this fertilization route is common in simultaneous hermaphrodites (Lange et al. 2013a), but it is currently unclear whether simultaneous hermaphroditism is itself a cause of this bias, as might be expected from theoretical predictions of a greater propensity toward escalated mate harm in hermaphrodites (Michiels and Koene 2006 see also Preece et al. 2009), or whether the pattern arises as a consequence of other common features of simultaneous hermaphrodites such as their tendency to be soft-bodied (Lange et al. 2013a) and/or to possess a high capacity for regeneration.


Parthenogenesis

Parthenogenesis is a form of asexual reproduction where an egg develops into a complete individual without being fertilized. The resulting offspring can be either haploid or diploid, depending on the process and the species. Parthenogenesis occurs in invertebrates such as water fleas, rotifers, aphids, stick insects, some ants, wasps, and bees. Bees use parthenogenesis to produce haploid males (drones) and diploid females (workers). If an egg is fertilized, a queen is produced. The queen bee controls the reproduction of the hive bees to regulate the type of bee produced.

Some vertebrate animals, such as certain reptiles, amphibians, and fish, also reproduce through parthenogenesis. Although more common in plants, parthenogenesis has been observed in animal species that were segregated by sex in terrestrial or marine zoos. Two Komodo dragons, a bonnethead shark, and a blacktip shark have produced parthenogenic young when the females have been isolated from males.


II. Food Chains and Food Webs

Trophic refers to eating or nutrition. In a typical trophic relationship, one organism eats all or part of another organism. In another type of trophic relationship, a decomposer consumes organic molecules from dead organic matter. A food chain summarizes a sequence of trophic relationships within an ecosystem.

One type of food chain begins with a producer:

Producer &rArr Primary Producer &rArr Secondary Consumer

Another type of food chain begins with dead organic matter:

Dead Organic Matter &rArr Decomposer &rArr Secondary Consumer

Organisms can be categorized in different trophic levels, e.g. producer, primary consumer or decomposer, and secondary consumer. If a consumer eats organisms at more than one trophic level, it is called a trophic omnivore. Trophic omnivores are a broad category that includes not only omnivores (animals that eat both plants and animals), but also some other types of organisms (see question 5 below).

Your teacher will supply your group with a deck of cards, each of which describes one type of organism that lives in Yellowstone National Park (plus a card for dead organic matter).

  • Find three cards that form a food chain that starts with a producer. Find three other cards that form a food chain that starts with dead organic matter. Arrange these on a sheet of paper and draw arrows to create two food chains.

The trophic relationships in real biological communities are much more complex than a simple food chain. These more complex trophic relationships are shown in a food web.


The diagram below shows a small part of a food web. Notice that the food web contains multiple food chains.

4. Circle the organisms in one of the food chains in this food web. Label the producer in this food chain.

5. Explain why the hawk in this food web is a trophic omnivore, even though it does not eat both plants and animals.

  • You will use all of the cards in your Yellowstone deck to create a Yellowstone food web. Begin by drawing the boxes shown in this chart on your lab table or on the large paper provided by your teacher.

  • Identify the producers and decomposers in your Yellowstone deck and put these cards in the appropriate boxes. Next, add the cards for the primary consumers and secondary consumers. Finally, put the cards for the trophic omnivores in the appropriate spaces between the boxes.
  • Draw an arrow to show each trophic relationship listed on the cards (42 arrows for the 42 trophic relationships).

6. After your teacher has checked and approved your food web, draw a diagram of the food web on a separate sheet of paper. Include all of the organisms and arrows.

Some scientists distinguish between a green food web that begins with producers and a brown food web that begins with dead organic matter. Notice that in your Yellowstone food web, the green food web contains more familiar plants and animals, whereas the organisms in the brown food web tend to be smaller and less familiar. Some organisms at higher trophic levels are part of both the green and brown food webs.

7. What problem or problems would occur if there were no decomposers and no brown food web?

Although your food web looks complex, a real biological food web is much more complex. Here are two of the reasons why a complete Yellowstone food web would be much more complex.

  • Your food web includes only 23 types of organisms. In contrast, Yellowstone Park has many more types of organisms, including more than 1000 different kinds of plants, more than 1000 different kinds of insects, many hundreds of other types of animals, and many types of fungi, Protista, and bacteria.
  • Most organisms have more trophic relationships than the few that are shown on each card.

Food webs can help us understand how changes in the population size of one organism in an ecosystem can influence the population size of another organism in the ecosystem. Humans eliminated wolves from Yellowstone National Park for most of the twentieth century. Gray wolves were reintroduced in the park in 1995-1996. The next page shows evidence that, after wolves were reintroduced, there were changes in the populations of some other organisms in Yellowstone.
The top two graphs show how the population of wolves and the population of elk changed following the introduction of wolves into Yellowstone National Park.

The third graph shows trends in the amount of growth of willows (data for annual growth ring size from two different studies).


8. For each organism in the table below:

  • State whether population size or amount of growth generally decreased, increased, or stayed the same.
  • Explain a likely reason for each trend. Use the information from the food web to understand the trends in the elk population and willow growth.

Trend in Population Size or Amount of Growth Explanation for this Trend
Wolves
Elk
Willow

If an increase in a predator population results in a decrease in an herbivore population which in turn results in an increase in plant growth, this type of effect is called a trophic cascade.


6 Answers 6

Does the text of Genesis rule out a theory that at least before Eve, Adam was not specifically and anatomically male?

There is a long tradition within Judaism, of reading the creation narrative and seeing the creation of humanity as a combination of male/female (androgynous). JEREMIAH BEN ELEAZAR is only one in a line of many. This idea is also found in other ANE thinking and confirmed archaeologically.

In recent years, the argument was taken up by feminist writer Phyllis Trible.

There are ambiguities in the scripture which is why we have seen more than 2000 years of disagreement from those who spoke the original Hebrew language. It is a matter of interpreting what is meant by an ambiguous text.

Said R’ Yirmiyah ben Elazar: In the hour when the Holy One created the first human, He created him [as] an androgyne/androgynous, as it is said, “male and female He created them”.

Here is an article that summarizes the argument nicely:

Reisenberger, Azila Talit. 1993. “The Creation of Adam as Hermaphrodite--and Its Implications for Feminist Theology.” Judaism 42 (4): 447.

As is usual in a Jewish interpretation, she surveys the different interpretations throughout the ages, but mainly leaves it open for you to decide.

She also mentions that many Jewish thinkers - like Philo - interpreted the story allegorically as the perfect picture of humanity is male/female. You need both sides to get an accurate depiction of humanity.

Another article surveys many of the archaeological finds from the near east:

Ziffer, Irit. "The First Adam, Androgyny, and the ʿAin Ghazal Two-headed Busts in Context." Israel Exploration Journal 57, no. 2 (2007): 129-52.

Here is a quote from Irit Ziffer regarding ANE thinking about early humanity:

"Historically speaking, androgyny symbolizes the perfect human being: female attributes cast into a male vessel. [from Third Dynasty of Ur - a statue of a king] This image expresses the king's perfection: not the robust, masculine bearded hero, but a more 'feminine' figure that incorporates male and female characteristics, thereby symbolizing humanity in its entirety" (pg. 140)

The article details out many more examples and notes that Philo and that a number of the Sages from the Midrashic and Talmudic period agreed.

My thought is that before we allow the arrogance of history to throw these ancient interpreters under the bus maybe we should provide an allowance that they didn't come up with this in only first-order thinking. We should examine it ourselves before we throw it away.

Having just read gen 1:27 in the Hebrew, I cannot see how someone could draw the stated conclusion without both eisegesis and textual strangulation. I observe the following about the three clauses of Gen 1:27 -

  • And God created human [= mankind masc. singular] in his image,
  • in the image of God He created him [= 3rd person masc. singular],
  • male [= masc. singular] and female [= fem. singular] He created them [3rd person masc. plural].

While the "mankind/human" in the first clause is masculine, that is precisely as one would expect for a noun like "humankind" indicating the genesis of the human race in Adam.

Indeed the very next verse we have:

Thus, in this first creation account of Gen 1, we have the creation of two people, male and female who are told to multiply.

The more detailed record in the second creation account of Gen 2:4f provides greater insights from which we learn:

  • Adam (v20) and God (v18) recognize his loneliness and that he needed a partner
  • Eve is created from Adam's side (V21, 22)

I am at a loss to understand how or why anyone might draw such unwarranted conclusions about an initially hermaphrodite Adam! Such a conclusion has escaped the notice of 2000 years of Bible interpreters warranting a good deal on suspicion.

No, for a few reasons I can think of.

(1) God said, "It is not good for man to be alone" (2:18). Unless we take God to be suggesting that he made a mistaken in making Adam without a partner, and did not rather create man without a partner only to show that he is more than the animals (2:20), this means man and woman was the original intention in creating Adam.

(2) The text says nothing about Adam being changed in the creation of Eve, but only that Eve was taken from his side (2:22).

(3) The "him" in 1:27 answers to "mankind," not to Adam alone, even as the plural "them" in 1:27b evinces.

No, as @SolaGratia so properly stated above, no mention is made of an alteration of the flesh of Adam. God's plan in verse 26 was no secret--no debacle--no failed attempt to "get it right. God, who "made" the plan in verse 26, began carying it out by using the very distinct process of *"creating" man and naming them, "Adam", according to Gen 1:27, KJV:

So God created man in his own image, in the image of God created he him male and female created he them. (My emphasis)

The word, "created" is used only three times in the creation narrative, 1) on day-one at a time that there was no heaven and earth 2) on day-five--life at a time when there was no living creature on earth 3)on day six at a time that there were no complex spirits that were both in God's image and after His complex likeness.

This creative act made no mention of a flesh, bone, and blood physical man. How could it have been any other way? Did God have a physical flesh, blood, and bone physical body at that time? Of course not. God is Spirit. Therefore, that is what God created. God's spirit is a single plurality of facets, faces, paniym (H6440), presences, or persons. Therefore, that is what God created--in "our "imageand after "our" likeness. Yet the plan was also to have "them" inhabit" the earth. Accordingly, Isaiah 43:1 declares:

But now thus saith the LORD that created thee, O Jacob, and he that formed thee, O Israel, Fear not: for I have redeemed thee, I have called thee by thy name thou art mine.

Even every one that is called by my name: for I have "created" him for my glory, I have 'formed" him yea, I have "made" him.

And, among many other such illustrations, Isaiah 45:15 further explains:

For thus saith the LORD that created the heavens God himself that formed the earth and made it he hath established it, he created it not in vain, he formed it to be inhabited: I am the LORD and there is none else. (My emphasis)

The "heaven and the earth" (a joint object of the preposition, created) was created on day-one (without form, and void--vanity--invisible--like gaseous matter), but later "made" and "formed" on distinctly different days following that creation project. Why did He physically alter that day-one invisible vain matter? Because He created it in faith, not in vain, as He declared above by the prophet, and as the Hebrew Fathers very much understood--even in the first century, according to Hebrews 11:3:

Through faith we understand that the worlds were framed by the word of God, so that things which are seen were not made of things which do appear.

The LORD does not have a stammering problem. If He says that he created and made it in the same sentence, or that he also formed it, He means exactly what He says. He did all those things.

**How important is the difference between "created", "made", and "formed"? Created (Strongs H1254) means to bring forth out of nothing. Artists are often reckoned as being creative, but never when their artifact is something that has been already accomplished. Moses's book of beginnings clearly distinguishes between the three words. Never, in the entire Scripture does the LORD say that He "formed" bodies of liquid waters. Nowhere does He say that He created "woman." Nowhere does He say that He created "Eve." The woman, and Eve always are attributed to bein "made" and "formed". But Adam, the created spirit, was also thereafter, made, and formed according to the plan in verse 26. He existed (only for a short period of time) on that very day he was created, as a male and female--a spiritual duality awaiting to become the "things hoped for", but not yet visible as being the evidence of things "not yet seen"--a man and a woman.

Genesis, Chapter two is primarily charged with describing the making and forming of the man, first, then the forming of the of the woman, as 1 Timothy 2:13 demands, according to that very Jewish Rabbi, Paul:

For Adam was first formed, then Eve.

Notice that, in Scripture, when in Christ, the man and the woman are treated without respect to their being male or female, according to Galatians 3: 28, though while on this earth, they are to be husband and wife:

There is neither Jew nor Greek, there is neither bond nor free, there is neither male nor female: for ye are all one in Christ Jesus.

Certainly, this is looking forward to our being neither married, nor given in marriage in the resurrection, as we see in Matthew 22:30:

For in the resurrection they neither marry, nor are given in marriage, but are as the angels of God in heaven.

So we will be individual unconnected spirits (as by marriage)--like the angels--but with our resurrected bodies. But Adam began as a "man", and Eve was made a "woman", not a "wohermaphrodite"

Many interpreters have pointed out that Genesis 1 and 2 are separate creation accounts. In the first, God speaks a word and creation proceeds from that. In the second, God gets his hands dirty and forms his creation out of the soil. Let's look at Genesis 1 first.

In the previous 5 days, God separates:

  1. Light from darkness.
  2. Water above and water below.
  3. Land and seas.
  4. Day from night.
  5. Creatures in the water from creatures in the sky. (The word "separate" isn't used here, but there is a parallel idea.)

On the sixth day he created creatures on the land "each according to its kind". Finally he created humankind. Now it is possible to read the Genesis 1:27 as God creating a species where each individual contains both male and female attributes. It would still fit into the theme of separation because the beasts are created "according to their kind" and humanity is created "in the image of God".

The NET Bible footnotes argue against that reading:

The Hebrew word is אָדָם (ʾadam), which can sometimes refer to man, as opposed to woman. The term refers here to humankind, comprised of male and female. The singular is clearly collective (see the plural verb, “[that] they may rule” in v. 26b) and the referent is defined specifically as “male and female” in v. 27. Usage elsewhere in Gen 1-11 supports this as well. In 5:2 we read: “Male and female he created them, and he blessed them and called their name ‘humankind’ (אָדָם).” The noun also refers to humankind in 6:1, 5-7 and in 9:5-6.—NET Bible footnote #48 on Genesis 1:26

In addition, the following verses give God's first words to humanity to "Be fruitful and multiply!" It seems unlikely that the ancient understanding of fertility would contemplate self-fertilization. Genesis as a whole is obsessed with the difficulty of reproduction and demonstrates both male and female sexes have responsibly to follow the commandment. Given the culture of the ancient Hebrews, the burden is on interpretations that introduce the hermaphrodite concept.

Now Genesis 2 could be a more detailed description of the sixth day or an entirely separate account. Unlike the first account, God seems to use an iterative process to produce humankind. He creates the man, then he creates animals and birds for the man to name and finally, when none of them served the purpose, God took a part of the man to use to form a woman. The story has an element of drama as we wait for the proper helper/companion/sustainer to be found. The suspense of the story comes from knowing that the man needs a woman, not another type of creature. The man needs someone who can help him be fruitful and multiply.

I don't know if there's a way to rule out an interpretation of the first person as a hermaphrodite grammatically, but it would cause many problems thematically. Genesis, at least in the form passed down to us, is obsessed with the drama of reproduction. For instance, the story of Isaac gains weight because we know the struggle of Abraham and Sara to conceive a son. It also seems a concept brought in from other cultures rather than a concept familiar to the ancient Hebrews.


Why There Are Only Two Sexes

A generation ago, this might have seemed like a silly question. But given the rise of gender theory, transgenderism, intersexuality, and all of their related phenomena, the question now appears to be both complex and pressing. . .

What differentiates human males from human females? Is it the number of sex chromosomes? Is it the possession of the appropriate sex organs? Is it the amount of testosterone or estrogen? The difficulty is that none of these standards always works: some individuals are born with extra chromosomes, such as XXYY or XYY. Some individuals are born with both pairs of sex organs. Some females have higher testosterone levels than many men.

Any single instance of an outlier counts as a serious objection to the binary sex distinction. Individual human beings are by nature either male or female just as by nature a number is either odd or even (by nature I mean the essence of a thing or what necessarily follows upon a thing’s essence). If one encountered even one number that is neither odd nor even, then this strange number would be enough to show that numbers are not “by nature either odd or even.” If one encountered even one triangle that was four-sided, this would be enough to show that triangles are not “by nature three-sided.” Similarly, if one encountered even one individual who did not fit the binary sex norm, then this single counterexample would be enough to disprove the traditional sex distinction.

Luckily, there are no non-odd-nor-even numbers. Nor are there no four-sided triangles, because four-sided triangles are a contradiction in terms. But is an intersex human being a contradiction in terms?

Biologically, intersex individuals seem to exist, as do people with other non-binary sex conditions. Hermaphrodites have male and female sexual organs. Some individuals with male organs have XX chromosomes. Some genetically male individuals have incomplete female sexual organs. What non-arbitrary but universal standard can there possibly be for determining sex?

What Determines Sex?

Our sex—male or female—is determined by our basic capacity to engage in sexually reproductive acts. Consider the following thought experiment by Christopher Martin:

Suppose we met a race of creatures—fairly clearly non-rational animals—that was very different from us: on Mars, say. And the question arises: are these creatures sexed? and if so, can we distinguish male and female? We need to think now how we would go about finding out these answers. We would not do it by investigating their psyches, nor even merely by just looking at (or cutting up) individuals. We would try to find out how they reproduced and what was the role of the different organs of the different individuals involved in reproduction. Thus, sex is a biological and teleological notion. Anything else which is called sexual is so called ultimately because it has some relation to this process, to these organs.

If we observe that the members of a species reproduce asexually, then we rightly conclude that neither male nor female exist in that species. But if we observe that two are required for reproduction to occur, we rightly conclude that the species reproduces sexually by the union of the two. We name these two types differently—as male and female—based upon the roles they play in reproduction. Such is why Aquinas held to a binary account of sex: “The distinction of the sexes is ordained in animals to the generation which occurs through coitus.” If human beings had no ordering to reproduction, or no sexual reproduction occurred, not only would one have no concept of gender, there would be no biological sex in human beings.

There, thus, can only be two biological sexes for human beings. In syllogistic form, what I am arguing is this:

  1. Biological sex is defined in relation to the roles played in sexual reproduction.
  2. Sexual reproduction involves only two, namely, male and female.
  3. Thus, biological sex is only two, namely, male or female.

Defects occur in nature, but defects imply a norm from which they deflect. A castrated man is still a male a female with a mastectomy is still a female. The fact that one is born with ambiguous genitalia does not do away with one’s true sex. That it is hard to identify someone as male or female does not mean one is neither. Identical twins are hard to distinguish, but they are still distinct persons. Epistemological problems need not entail ontological ones.

Consider the case of plants that reproduce sexually. When we discover a plant missing parts of its sexual organs, we do not thereby conclude that we have discovered a third sex. Rather biologists rightly concur that what you have found is a defective plant. Likewise, in human beings, when one has an extra chromosome, or defective genitalia, you have just that: a sexual defect at the physical level. Such people often are wonderful, loving, and morally upright persons, but physically something has gone wrong.

Hermaphrodites are individuals with both pairs of sex organs. While in very rare cases some human beings have both pairs of genitalia, in no case whatsoever has it ever been observed that both pairs are fully functioning. True human hermaphrodites with both male and female sexual organs that fully function don’t exist. Such is why no cases of self-fertilization have ever been recorded in human beings.

Even if we did discover an individual human being with both pairs of fully functioning sex organs, such a case would not disprove the binary distinction. What you would have is someone who is both male and female one who is able to act either as male or female depending upon the other sex with which that individual desired to reproduce. Hermaphroditism, rather than disproving the traditional binary distinction, actually reinforces it. We would not even know hermaphrodites existed, let alone be able to speak of them, unless we knew of the male-female binary.

Differentiating Potencies

How we fundamentally distinguish male and female then is based upon the two biological roles in reproduction. A human individual that has the basic capacity to reproduce with the female is biologically and truly a male. A human individual that has the basic capacity to reproduce with a male is biologically and truly a female. Male and female are defined in reference to each other, which is why they are correlative terms.

One must distinguish, however, between two types of “capacity.” Males are still males even when they are not actively reproducing with a female, or if they are unable to reproduce due to sterility, castration, or a genetic or physical defect. The sense of “capacity” or “potency” in question here is a fundamental one. A mechanic that doesn’t have the proper tools is still “capable” of fixing your car, but not in the same way in which a mechanic with the proper tools is “capable” to fix your car in the here and now. A male is the type of organism that is capable to impregnate the female. In other words, he could impregnate her, given that he has the appropriate functioning organs. A female, however, cannot impregnate another female.

For the sake of argument, let us grant that it might be physically possible for a female to have a complete sex change operation that she had a fully functioning male genitalia, male hormones, and male chromosomes that were fully integrated into her body. In this case she would cease to be female, but become a male. Even if complete sex change operations were possible (which they will most likely never be), such operations would be no argument against the traditional binary distinction. In such a case, the woman would not become a third sex she would cease to be female and become a male.

Given that human beings reproduce sexually, they are biologically either only male or female. Men are men, and women are women. True hermaphrodites with fully functioning sexual organs do not exist in human beings. There is no tertium quid.


Why Are There So Many More Species on Land When the Sea Is Bigger?

Most of the Earth’s surface is ocean. Life began there. But marine life accounts for only 15 percent of the world’s species.

Half a billion years ago on Earth, after the Cambrian explosion had created an astonishing array of new species, there was still no life on land. No complex life anyway. No plants, no animals, certainly nothing that even compared to the great diversity of life in the sea, which teemed with trilobites, crustaceans, bristly worms, and soft squid-like creatures. Most major animals groups that exist today originated in the sea at this time.

Fast forward to the present, and it is now the land that has a dizzying array of species. In particular: flowering plants, fungi, and insects, so many damn insects. By one estimate, there are five times as many terrestrial species as marine species today. So how did biodiversity in the ocean—despite its head start, despite its larger share of the Earth’s surface area—come to fall so far behind biodiversity on land?

Why more species live on land than in the ocean has puzzled biologists for a long time. Robert May, a ecologist at the University of Oxford, appears to be the first to put the conundrum down in writing in a 1994 article titled, “Biological Diversity: Differences between Land and Sea (and Discussion).”

The question has held for the two decades since, even as humans have explored more and more of the deep ocean. Scientists now estimate that 80 percent of Earth’s species live on land, 15 percent in the ocean, and the remaining 5 percent in freshwater. They do not think this difference is entirely an artifact of land being better explored. “There are oodles and oodles of species in the sea, but to make up that difference would take an awful lot,” says Geerat Vermeij, a marine ecologist and paleoecologist who has written about the land-sea species discrepancy with his collaborator Rick Grosberg, another ecologist at the University of California, Davis. So this seeming lack of ocean diversity is not just the bias of us land-based creatures, Vermeij and Grosberg argue—a bias that they as marine researchers are all too keenly aware of.

What then is intrinsically different about the land’s ability to support biodiversity?

(We’re going to put aside microbial diversity in this discussion, which is not meant as a slight to microbes. But rather, they are too different to generalize together with multicellular life. Single-celled microbes are governed by different forces and even the concept of “species” is different. They deserve their own discussion.)

One reason May and others since have suggested is the physical layout of terrestrial habitats, which may be both more fragmented and more diverse. For example, as Charles Darwin famously documented in the Galapagos, islands are hotbeds for diversification. Over time, natural selection and even chance can turn two different populations of the same species on two islands into two species. The ocean is, in contrast, one big interconnected body of water, with fewer physical barriers to keep populations apart. It also doesn’t have as many temperature extremes that can drive diversification on land.

Land may also be “architecturally elaborate,” to use May’s term. Forests, for example, have covered much of the Earth’s land surface, and the leaves and stems of trees create new niches for species to exploit. Coral do the same in the ocean, of course, but they do not cover nearly as much of the seafloor.

Plants definitely play a major role. The Earth’s tipping point from predominantly marine to terrestrial life came around about 125 million years ago, during the Cretaceous period, where early flowering plants evolved to be extraordinarily successful on land. Plants need sunlight for photosynthesis, but there’s little sun in the ocean outside of shallow coastal areas. For this reason, land is simply more productive that the cold, dark depths of the sea. “The deep sea is basically a big fridge with the door closed for a long time,” says Mark Costello, a marine biologist at the University of Auckland, who recently published an overview of marine biodiversity. Sure there is life in the deep sea, but not nearly as much as on the sunny coast and land.

Interestingly, Costello notes, increased productivity on land after the diversification of flowering plants also seems to have fed back into increased diversity in the oceans. Pollen, for example, can be an important source of food on the floor of the deep sea. A recent study found pollen likely from pine plantations in New Zealand in a deep sea trench 35,000 feet below the surface of the Pacific Ocean.

The diversification of flowering plants also has everything to do with their coevolution with insects. Plants, for example, evolved features like flowers with long tubes that could only be reached by long-tongued bees that pollinate them. “It’s kind of a big race between the plants and the insects,” says Costello. This coevolution helped create an astonishing number of species: The vast majority of plants on Earth are flowering plants, and the vast majority of animals on Earth are insects. By one estimate, insects alone account for 80 percent of all species on the planet.

Yet insects, so successful on land, are marginal in the sea. Vermeij and Grosberg trace the lack of diversity among small animals to the differences in air and water as a medium. Small animals, like an insect, have more difficulty moving around in water because it is thicker than air. (This applies less so to bigger animals due to the laws of physics.) Mating scents and even visual information don’t travel as well through water—limiting the potential for sexual selection to drive diversification. Sexual selection drives traits that may not seem beneficial but for whatever reasons are preferred by mates. The peacock’s tail is a classic example.

Drawing on the work of Richard Strathmann, Vermeij and Grosberg also try to get at why something like the relationship between flowering plants and insects could not exist in the ocean. The seawater is teeming with potential food sources like zooplankton. While going from one hypothetical sea flower to another, a marine creature would encounter plenty of food floating in the water along the way. Why swim all the way to the other sea flower? On the other hand, an insect flying from one flower with nectar to another would just be flying through air. There is no food floating in the air. And this has evolutionary consequences: A hypothetical sea flower would have to offer much more nectar to attract pollinators lazily feeding on floating food—so much so that it’s not worth it.