How does antagnostic coevolution work in ducks?

How does antagnostic coevolution work in ducks?

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I recently learned that in ducks, the penis and vagina have coevolved: the vagina of the female ducks gets dead-end sacs and clockwise coils; the penis of male ducks become longest and its morphology changed to adapt to the female vagina. [1] This antagnostic coevolution happened due to the evolutionary arms race between male and female ducks.

This seems counter-intuitive when we think about natural selection. Indeed, if female ducks are forcibly copulated, they are more susceptible to reproducing themselves and sharing their genetic traits.

From [2], it appears that only 3% of forced copulations results in fertilization. If this is the case, why has the male phallus evolved this way? Indeed, it does not appear to me to be a good evolutionary strategy.

If [1] and [2] are correct, I would think that the duck vagina and phallus shouldn't have coevolved that way. What am I missing?

[1] Brennan, P. L., Prum, R. O., McCracken, K. G., Sorenson, M. D., Wilson, R. E., & Birkhead, T. R. (2007). Coevolution of male and female genital morphology in waterfowl. PLoS one, 2(5), e418.

[2] Burns, J. T., Cheng, K. M., & McKinney, F. (1980). Forced copulation in captive mallards. I. Fertilization of eggs. The Auk, 97(4), 875-879.

Rogue Sperm Indicate Sexually Antagonistic Coevolution in Nematodes

Intense reproductive competition often continues long after animals finish mating. In many species, sperm from one male compete with those from others to find and fertilize oocytes. Since this competition occurs inside the female reproductive tract, she often influences the outcome through physical or chemical factors, leading to cryptic female choice. Finally, traits that help males compete with each other are sometimes harmful to females, and female countermeasures may thwart the interests of males, which can lead to an arms race between the sexes known as sexually antagonistic coevolution. New studies from Caenorhabditis nematodes suggest that males compete with each other by producing sperm that migrate aggressively and that these sperm may be more likely to win access to oocytes. However, one byproduct of this competition appears to be an increased probability that these sperm will go astray, invading the ovary, prematurely activating oocytes, and sometimes crossing basement membranes and leaving the gonad altogether. These harmful effects are sometimes observed in crosses between animals of the same species but are most easily detected in interspecies crosses, leading to dramatically lowered fitness, presumably because the competitiveness of the sperm and the associated female countermeasures are not precisely matched. This mismatch is most obvious in crosses involving individuals from androdioecious species (which have both hermaphrodites and males), as predicted by the lower levels of sperm competition these species experience. These results suggest a striking example of sexually antagonistic coevolution and dramatically expand the value of nematodes as a laboratory system for studying postcopulatory interactions.

On the Origin of Species focused almost exclusively on the role of natural selection in evolution [1], but Darwin realized that animals also compete for mates and described the process of sexual selection at length in a later book [2]. The simplest examples involve combat like that between male elephant seals fighting for access to females. However, sexual selection also includes many other types of interactions. For example, some male birds have elaborate plumage because females favor this trait when choosing mates (reviewed in [3]). In their simplest form, these interactions can be thought of as parts of a triangle𠅌ompetition between two males forming the base and the interactions between each of the males and the female forming the two legs.


Antagonistic interactions between the sexes are important drivers of evolutionary divergence. Interlocus sexual conflict is generally described as a conflict between alleles at two interacting loci whose identity and genomic location are arbitrary, but with opposite fitness effects in each sex. We build on previous theory by suggesting that when loci under interlocus sexual conflict are located on the sex chromosomes it can lead to cycles of antagonistic coevolution between them and therefore between the sexes. We tested this hypothesis by performing experimental crosses using Drosophila melanogaster where we reciprocally exchanged the sex chromosomes between five allopatric wild-type populations in a round-robin design. Disrupting putatively coevolved sex chromosome pairs resulted in increased male reproductive success in 16 of 20 experimental populations (10 of which were individually significant), but also resulted in lower offspring egg-to-adult viability that affected both male and female fitness. After 25 generations of experimental evolution these sexually antagonistic fitness effects appeared to be resolved. To formalize our hypothesis, we developed population genetic models of antagonistic coevolution using fitness expressions based on our empirical results. Our model predictions support the conclusion that antagonistic coevolution between the sex chromosomes is plausible under the fitness effects observed in our experiments. Together, our results lend both empirical and theoretical support to the idea that cycles of antagonistic coevolution can occur between sex chromosomes and illustrate how this process, in combination with autosomal coadaptation, may drive genetic and phenotypic divergence between populations.

Sex chromosomes have a number of unique properties that distinguish them from autosomes, and one another, including their mode of inheritance, the selection experienced in the two sexes, and gene content (1). These processes are interdependent and strongly influence the genetic variation harbored on each sex chromosome. The Y chromosome is inherited exclusively through males and is therefore exposed only to selection in males. Because the Y chromosome is male limited, any Y-linked genetic variation that is not male beneficial should experience purifying selection, which is consistent with empirical results (2 ⇓ –4). In contrast, although the X chromosome is not sex limited, it still experiences different selection pressures than both the autosomes and the Y chromosome (1). The X chromosome is largely exposed to selection in females as it spends two-thirds of its time in females (1), but it is also always exposed to selection when present in males since it is hemizygous in males, (i.e., X-linked genes are unsheltered by dominance effects in males) (5). Hence, whether genes on the X chromosome are female or male beneficial can depend on the dominance coefficient (6). Collectively, these unique properties have made sex chromosomes important factors in two major fields within evolutionary biology: speciation (7) and sexual conflict (1, 8).

Here we aimed to investigate whether interactions between sex chromosomes contribute to between-population divergence at the intraspecific level, as has previously been shown in interspecific comparisons (7). To do so, we performed experimental crosses to “swap” either an X or a Y chromosome between five geographically isolated wild-type populations of Drosophila melanogaster, allowing us to investigate the effects of novel interactions between the sex chromosomes on male reproductive fitness. As we outline below, we expected males carrying a novel sex chromosome to experience changes in reproductive success of opposite sign, depending on whether the source populations happen to accumulate incompatibilities that involve the Y or the incompatibilities are driven by sexually antagonistic selection.

When two allopatric populations diverge, each will accumulate unique genetic mutations scattered throughout the genome that may not affect the fitness in either population on their own, but may affect the sterility and viability of hybrid offspring if the two populations come into secondary contact (e.g., the Dobzhansky–Muller model of postzygotic isolation) (9, 10). Because the Y chromosome in Drosophila is inactive in somatic cells (11), it is more likely that Y-linked incompatibilities will cause sterility than reduced viability, which has been documented in multiple Drosophila species crosses (summarized in ref. 12). We therefore expected to find evidence of sterility or decreased fertility in males if mutation accumulation on the Y chromosome were an important factor in population divergence in this species. We found no such evidence (Results) and conclude that accumulation of sex-linked incompatibilities influencing male sterility has not been a major contribution to divergence in our five wild-type populations.

Alternatively, sexually antagonistic coevolution between the sex chromosomes could, in principle, provide a mechanism for the sex chromosomes to contribute to evolutionary divergence between populations (13), as suggested by studies of Y-linked regulation of autosomal gene expression (14). The theory of sexually antagonistic coevolution is based on the Red Queen process (15). In short, when males increase their reproductive success through an adaptation that is simultaneously detrimental to females, it creates selection for a counter-adaptation in females to regain their lost fitness. The process may be repeated in multiple cycles over evolutionary time until a resolution is reached or a palliative adaptation ends the conflict (16, 17). Sexually antagonistic coevolution can be considered a form of interlocus sexual conflict (13) if the traits involved are encoded by different genes in males and females (18). As first proposed by Rice and Holland (13) in 1997, when the loci in question are located on the sex chromosomes, this could lead to cycles of sexual antagonistic coevolution between the sex chromosomes. Depending on the relative sizes of the sex chromosomes and autosomal genome, and the extensive regulatory function of sex-linked genes, these cycles could of course also result in coadaptation with the autosomes.

There are three different ways that a Y-linked male-beneficial allele could harm females and possibly generate sexual conflict: 1) The allele could recombine onto the X and harm female carriers, 2) the allele could cause males to limit females’ mating opportunities (e.g., by harming them), or 3) the allele could harm offspring. Scenario 1 is not relevant for our experimental results because recombination does not occur in D. melanogaster males and there are no pseudoautosomal regions on the sex chromosomes hence there is no opportunity for a Y-linked allele to recombine onto an X chromosome (19, 20). Scenario 2 appears inconsistent with our empirical findings (Results) but could potentially result in similar coevolutionary cycles caused by conflict over mating opportunities, which we explore further in SI Appendix, section C. Hereafter, we focus on scenario 3. If a Y-linked male-beneficial mutation arises that increases male reproductive success but decreases offspring fitness, it should spread through a population because it is subject to selection in males only. The sexually antagonistic male-beneficial mutation creates selection favoring compensatory mutations that might arise on the X chromosome or autosomes to restore female fitness again (e.g., by increased survival of her offspring). Several mechanisms could potentially generate such sexual conflict over offspring survival in Drosophila. For example, male Drosophila can bias paternity by delivering seminal-fluid proteins that induce accelerated egg laying by females (21), potentially resulting in smaller eggs and therefore reduced offspring viability (22). A Y-linked allele influencing expression of seminal-fluid proteins could therefore create compensatory selection for resistance to accelerated egg laying, which would be disadvantageous alone. Similarly, a Y-linked allele that increases a male’s performance in sperm competition (e.g., by improving sperm displacement) could also cause increased offspring mortality due to polyspermy (23).

The specific mutations causing sexual conflict will likely differ between allopatric populations, and we would therefore expect to find an increase in male reproductive fitness when a Y chromosome with male beneficial mutations is paired with an X chromosome without the corresponding compensatory mutation(s). According to the sexually antagonistic coevolutionary model, we also predict a decrease in female fitness when mating with males harboring a Y chromosome paired to a novel X chromosome.

Another corollary of the antagonistic coevolutionary model is that the effect of disrupting coevolved sex chromosomes on male and female fitness should decay over subsequent generations as new compensatory mutations arise or novel combinations of segregating alleles achieve a similar compensatory effect. We tested this prediction by examining male and offspring fitness in our experimental populations after 25 generations of experimental evolution.

To complement our empirical results and help formalize the hypothesis of sexually antagonistic coevolution between the sex chromosomes, we developed population genetic models describing the evolution of two interacting loci located in different genomic regions (i.e., unlinked): a Y-linked locus influencing both adult male fertilization success (i.e., sperm competition) and subsequent offspring survival and a compensatory locus affecting only offspring survival located on either an autosome or the X chromosome.

Stage 1: Create a Laboratory Island Population

The study of island populations has played an important role in the study of evolution, beginning with the pioneering studies of Charles Darwin and Alfred Wallace. It is our view that one of the major reasons that island populations have been particularly informative is that they are much simpler then continental populations (in the context of both biotic and abiotic factors) and therefore easier to understand. Laboratory populations represent island populations that conveniently reside within the laboratory where joint measurements of fitness and genetic variation are more feasible. They are far simpler than natural island populations, but this simplicity provides tractability in the context of evolutionary analysis. By comparison, ecologists have gained important insights into the extinction and colonization process by studying very small island populations of vertebrates in nature, despite the fact that these “islands” are little more than large protruding rocks, 1-16 m on a side (see, for example, ref. 41).

The utility of using laboratory populations to study evolution depends upon how much their evolution is regulated by the same principles that control the evolution of natural populations. Most past laboratory studies of D. melanogaster have used highly inbred stocks such as Oregon-R, Laussan-S, and Canton-S, or genetic samples that have been recently derived from nature and therefore have not adapted to the laboratory environment. In the latter case, the flies are tested in a novel environment so measures such as heritability and selection on the standing, heritable phenotypic variance are difficult to interpret. Inbred laboratory stocks lack these problems, but they have been bottlenecked many times, their extreme and uncontrolled crowding interferes with many forms of behavioral interactions that have historically been important in the species, and their laboratory culture varies among laboratories and stock centers. As a consequence, these inbred laboratory populations have evolved under crowded, uncontrolled conditions that preclude the importance of the rich repertoire of behavioral interactions within and between the sexes, and they have undoubtedly fixed for large numbers of deleterious alleles. To avoid these undesirable aspects of standard laboratory stocks, our laboratory, like others (e.g., the laboratories of Brian Charlesworth, Linda Partridge, and Michael Rose), has started a new laboratory population. The large outbred laboratory population that we study (LHM) was founded by Larry Harshman (now at the University of Nebraska) from 400 inseminated females collected in an orchard near Modesto, California in 1991. Since then, it has been maintained at a large effective population size (>1,800 breeding adults). In 1995 the population density of juveniles and adults was reduced so that juvenile density was consistently maintained at between 150-200 individuals per vial, and adult density was reduced further to only 16 pairs per vial (placed on its side to allow more horizontal space for the flies to spread-out). The low adult density increased the potential for behavioral interactions to contribute the adult fitness of both sexes.

The population of flies pass through three sets of 56 10-dram vials during their 2-week generation cycle. On day 1, the eggs that were laid at the end of the previous generation are randomly reduced to 150-200 per vial to prevent the extreme crowding that occurs in most mass-transfer laboratory cultures. The flies remain in these “juvenile competition” vials for 12 days during which larval competition, pupation, and the early adult stages occur. On day 12, the flies are mixed among vials and, after being randomly culled to 16 pairs per vial, are transferred to new “adult competition” vials where they reside for 48 h. Live yeast (10 mg) is applied to the top of the 10 ml of killed yeast medium in each vial. There is a steep linear relationship between the amount of live yeast applied and average female fecundity, indicating that live yeast is the major factor limiting female fecundity (42). In the adult competition vials, females compete intensely for the limited supply of live yeast, and males compete to inseminate females and fertilize their eggs. Eighteen hours before the end of the two-week generation cycle, the flies are transferred to “oviposition vials” (with no live yeast added), and the eggs laid at this time are used to begin the next generation. As a consequence, egg production in the oviposition vials represents the lifetime offspring production of both sexes. Put another way, the flies are selected to be “big-bang” reproducers, analogous to semelparous salmon. During the 2-week generation cycle, adults live for at most 6 days, and there is virtually no adult mortality during this time however, larval mortality does occur in the juvenile competition vials at a rate of ≈10% (43). In the following sections, all measurements of lifetime fitness and phenotypic traits are taken under conditions that closely match those of the routine culture of the LHM base population.

For the purpose of assaying the flies for lifetime fitness and other traits such as sperm displacement, we also have back-crossed genetic markers [brown eye (bw), brown-eye-dominant (bw D ), and nubbin wings (nub 2 )] and a compound-X [C(1)DX y f] into the LHM base population. Each marker or chromosome has been backcrossed a minimum of 10 times through the LHM base population. Only the brow-eyed (LHM-bw) and compound-X (LHM-DX) replicas of the LHM base population were used in the assays described below.

At the time of this writing, the LHM population has adapted to the laboratory, at continuous large effective size, for 350 generations. With such a long period to adapt to the laboratory environment, most polygenic quantitative traits should have had sufficient time to at least approach their new optima. The capacity for rapid evolution to a new environment is manifest in newly derived Drosophila populations (for example, see ref. 44) and is also illustrated by the transplantation experiments of Reznick et al. (45) in which natural populations of guppies were shown to rapidly adapt to new environments under field conditions. Because the LHM population has such a long history of adaptation to a prescribed laboratory environment, we are able to measure both its genetic and fitness variation in the environment to which it is adapted, and thereby assess antagonistic coevolution within and between the sexes. Because the model organism is D. melanogaster, we can apply the powerful set of genetic tools available only in this species to take full advantage of the laboratory island population.

Are you Scicurious?

Sci is going to so some selfish Friday Weird Science today. Selfish, because this article isn’t new, and was reported on by one of the GREATS. This guy. He (of course) did a completely brilliant job, and when he talked about it at SciOnline this past weekend, Sci was compelled to go and see the material for herself. And it’s something to SEE. And so see it you shall.
The reason this is selfish is because Sci knows it’s been reported on before. She wants to do it her ownself, as an excuse to read and understand the paper. And an excuse to giggle about it while she blogs it. There’s that, too.
Images below the cut NSFW, especially if you work with ducks.
Brennan, Clark, and Prum. “Explosive eversion and functional morphology of the duck penis supports sexual conflict in waterfowl genitalia” Proceedings of the Royal Society B, 2009.

There were a couple of things that Sci learned from this paper:
1) ducks are one of the few types of birds to have a penis (it’s a typical formation in waterfowl). This is because, in most species, semen is ejected from the cloaca of a male into the cloaca of a female (they touch cloacae to do this, in what’s called a “cloacal kiss”).

A bird cloaca. It’s a little hard to see, but the tail feathers are stick up at the top, feet are at the bottom. And in the middle is the hole.
In male ducks, however, it’s a little different. They have a penis which enters the cloaca and oviduct of the female, and the semen comes out the tip. Like ya do.
2) the penises of waterfowl are not made erect by blood flow, but by LYMPH. During erection, lymph fluid accumulates in the penis and makes it extend outward. Crazy, huh? Lovin’ that convergent evolution.
So why, you might ask, do ducks have a penis? If other birds don’t really seem to need it, why do ducks? The hypothesized answer is that a lot of copulation (that’s sex) in ducks is actually FORCED. The girls are not enthusiastic, and the males have to find a way to hold them down.
And this is where evolution comes in. It’s not a good idea for the females to just be having any dude’s babies, she wants to make sure she gets the fittest duck of the bunch. So she wants to make her oviduct access more difficult. In the case of ducks, it means that, while the males penis comes out in a spiral in ONE direction, the female’s oviduct has evolved to spiral THE OTHER WAY, as you can see here:

The spiral that comes out for the males can be almost the length of the entire duck!
Not only that, the female’s oviduct has lots of little blind ends and pouches off the end of it, making it easy for the male’s penis to get stuck in blind ends, or to not penetrate successfully at all. In return, the male’s penis is flexible, allowing him to bend around and try to get through the backwards shape. This phenomenon of sex one-upmanship is called antagonistic coevolution. To prove that this does happen in ducks, the authors of this study did slow motion video capture of duck penises. Not only that, they did slow motion capture of duck penises going into tubes of various shapes, so show that the antagonistic evolution of the female’s oviduct presented a mechanical barrier to the male duck.
Their data is self-evident:

(I think that would be SO much better if there was a hardcore electric guitar riff going on in the background).
Note the semen coming out at the tip of the penis (there’s some fluid at the base that I mistook for semen at first). This process is slowed down in the video, but in reality takes 1/3 of a SECOND. EXPLOSIVE. *BAM*.
They they had the ducks do their thing into a series of tubes. They started with silicone tubes, but ended up switching to glass, because the duck’s penises were so powerful they BROKE the silicone tubes:

(This one I think needs more heroic music. Something with trumpets.)
So why would female ducks have evolved so many barriers? This way, when they are forced into copulation, the males forcing them won’t get as far in, and will be delivering sperm nearer the cloaca. When the female pair bonds to the mate of her choice, on the other hand, she’ll be more cooperative (or at least not trying to dunk him or fly off), and he’ll get further up the oviduct and have a higher chance of making sure the babies are his.
There is also a possibility that the females can store sperm from the other males in the little pouches off their oviducts, but this seems kind of unlikely. Females bond to the men of their choice long before the breeding season begins, and so it is not in their interest to get some other dude’s babies in there. But this still should be tested (and given the depth of Brennan’s work in the duck, it might well be tested).
So there you have it, the twisted evolution of the duck penis.
Brennan, P., Clark, C., & Prum, R. (2009). Explosive eversion and functional morphology of the duck penis supports sexual conflict in waterfowl genitalia Proceedings of the Royal Society B: Biological Sciences DOI: 10.1098/rspb.2009.2139

This study is supported by the Strategic Priority Research Program of Chinese Academy of Sciences (XDB31000000), the National Natural Science Foundation of China (31822050 and 31821001), the Frontier Key Project of Chinese Academy of Sciences (QYZDY-SSW-SMC019), and the Youth Innovation Promotion Association, CAS (2016082). We thank Yixiang Shi and Long Huang for help with genomic data analysis and thank Chenglin Zhang, Hongshuai Shang, Yanqiang Yin, and Yunfang Xiu for help with sample collection.

Author Contributions

F.W. conceived and supervised this study. Y.H. performed the sample collection. Y.H., Lij.Y., and H.F. conducted the genomic data analyses. F.W., G.H., Q.W., Y.N., S.L., and Li Y. were involved in the project implementation and data interpretation. Y.H., Lij.Y., and F.W. wrote the manuscript with input from other authors.

Data Availability

The sequence data and the genome assembly of Baylisascaris schroederi have been deposited at NCBI under BioProject ID PRJNA612649. The sequence data and the genome assembly of Baylisascaris ailuri have been deposited at NCBI under BioProject ID PRJNA612650. The sequence data and the genome assembly of Toxascaris leonina have been deposited at NCBI under BioProject ID PRJNA612651.


Pedagogical studies in biology and general science emphasize the efficacy of hands-on, inquiry-based activities that actively engage students in the learning process (Hake 1998 Alters and Nelson 2002 Smith et al. 2005 Nelson 2008). We have described a game in which students work cooperatively in small groups to generate their own data for an independent test of the central prediction of the Red Queen Hypothesis. In pursuing this specific goal, students personally engage with the broader concepts of rapid coevolution and frequency-dependent selection. We offer this basic exercise as a fun and inexpensive tool for teaching evolution at the undergraduate and advanced high school level.

Explosive eversion and functional morphology of the duck penis supports sexual conflict in waterfowl genitalia

Coevolution of male and female genitalia in waterfowl has been hypothesized to occur through sexual conflict. This hypothesis raises questions about the functional morphology of the waterfowl penis and the mechanics of copulation in waterfowl, which are poorly understood. We used high-speed video of phallus eversion and histology to describe for the first time the functional morphology of the avian penis. Eversion of the 20 cm muscovy duck penis is explosive, taking an average of 0.36 s, and achieving a maximum velocity of 1.6 m s −1 . The collagen matrix of the penis is very thin and not arranged in an axial-orthogonal array, resulting in a penis that is flexible when erect. To test the hypothesis that female genital novelties make intromission difficult during forced copulations, we investigated penile eversion into glass tubes that presented different mechanical challenges to eversion. Eversion occurred successfully in a straight tube and a counterclockwise spiral tube that matched the chirality of the waterfowl penis, but eversion was significantly less successful into glass tubes with a clockwise spiral or a 135° bend, which mimicked female vaginal geometry. Our results support the hypothesis that duck vaginal complexity functions to exclude the penis during forced copulations, and coevolved with the waterfowl penis via antagonistic sexual conflict.


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When George Williams first proposed his theory of antagonistic pleiotropy in 1957, he concocted a hypothetical example of a gene that hastened the calcification of arteries during development but led to the calcification of arterial walls in later life. He did this because there were no genes known to have the rather odd characteristic of being beneficial in early life but detrimental later on. In the past 20 or so years, molecular biology has presented us with a cornucopia of such genes, and of nine predictions Williams made about senescence and aging, six have proven correct over the last six decades [ 4]. Ironically, it is the other sort of antagonistic pleiotropy, late life benefits at the expense of early life decrements that are now in the forefront of aging research.

We have barely touched the surface of a very large topic here. But it is a topic that should have increasing interest moving forward because aging biology is on the verge of some major advances. From current evidence, antagonistic pleiotropy is somewhere between very common or ubiquitous throughout the animal world (and though not discussed here, except briefly in yeast, potentially all living domains). Whenever an allele or new mutation is discovered to extend life, some detrimental effect on early life fitness is almost always observed. This explains why longevity alleles are not favored in wild populations. However, while antagonistic pleiotropy appears to be nearly ubiquitous, a majority of actual antagonistically pleiotropic alleles remain undiscovered in natural populations, and laboratory studies that describe alleles that extend lifespan often do not report early fitness effects. These gaps in our knowledge still need to be addressed, and we predict that results from both will provide even more compelling evidence for the antagonistic pleiotropy theory of aging. One finding that has emerged in recent years that is particularly reassuring for those of us seeking medical interventions to prolong human health is that such interventions often do not have to be deployed until relatively late in life—after reproduction is finished [ 69]. In these cases, whether there would have been antagonistically pleiotropic side effects in early life is moot. Thus, evolutionary biology does not preclude the possibility of medical interventions in the aging process.

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