Patricia L. R. Brennan

Coevolution of Male and Female Genital Morphology in Waterfowl

Most birds have simple genitalia; males lack external genitalia and females have simple vaginas. However, male waterfowl have a phallus whose length (1.5–>40 cm) and morphological elaborations vary among species and are positively correlated with the frequency of forced extra-pair copulations among waterfowl species. Here we report morphological complexity in female genital morphology in waterfowl and describe variation vaginal morphology that is unprecedented in birds. This variation comprises two anatomical novelties: (i) dead end sacs, and (ii) clockwise coils. These vaginal structures appear to function to exclude the intromission of the counter-clockwise spiralling male phallus without female cooperation. A phylogenetically controlled comparative analysis of 16 waterfowl species shows that the degree of vaginal elaboration is positively correlated with phallus length, demonstrating that female morphological complexity has co-evolved with male phallus length. Intersexual selection is most likely responsible for the observed coevolution, although identifying the specific mechanism is difficult. Our results suggest that females have evolved a cryptic anatomical mechanism of choice in response to forced extra-pair copulations.

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.

Ultraviolet visual sensitivity in three avian lineages: paleognaths, parrots, and passerines

Ultraviolet (UV) light-transmitted signals play a major role in avian foraging and communication, subserving functional roles in feeding, mate choice, egg recognition, and nestling discrimination. Sequencing functionally relevant regions of the short wavelength sensitive type 1 (SWS1) opsin gene that is responsible for modulating the extent of SWS1 UV sensitivity in birds allows predictions to be made about the visual system’s UV sensitivity in species where direct physiological or behavioral measures would be impractical or unethical. Here, we present SWS1 segment sequence data from representative species of three avian lineages for which visually based cues for foraging and communication have been investigated to varying extents. We also present a preliminary phylogenetic analysis and ancestral character state reconstructions of key spectral tuning sites along the SWS1 opsin based on our sequence data. The results suggest ubiquitous ultraviolet SWS1 sensitivity (UVS) in both paleognaths, including extinct moa (Emeidae), and parrots, including the nocturnal and flightless kakapo (Strigops habroptilus), and in most, but not all, songbird (oscine) lineages, and confirmed violet sensitivity (VS) in two suboscine families. Passerine hosts of avian brood parasites were included both UVS and VS taxa, but sensitivity did not co-vary with egg rejection behaviors. The results should stimulate future research into the functional parallels between the roles of visual signals and the genetic basis of visual sensitivity in birds and other taxa.

The limits of sexual conflict in the narrow sense: new insights from waterfowl biology.

Sexual conflict occurs when the evolutionary interests of the sexes differ and it broadly applies to decisions over mating, fertilization and parental investment. Recently, a narrower view of sexual conflict has emerged in which direct selection on females to avoid male-imposed costs during mating is considered the distinguishing feature of conflict, while indirect selection is considered negligible. In this view, intersexual selection via sensory bias is seen as the most relevant mechanism by which male traits that harm females evolve, with antagonistic coevolution between female preferences and male manipulation following. Under this narrower framework, female preference and resistance have been synonymized because both result in a mating bias, and similarly male display and coercion are not distinguished. Our recent work on genital evolution in waterfowl has highlighted problems with this approach. In waterfowl, preference and resistance are distinct components of female phenotype, and display and coercion are independent male strategies. Female preference for male displays result in mate choice, while forced copulations by unpreferred males result in resistance to prevent these males from achieving matings and fertilizations. Genital elaborations in female waterfowl appear to function in reinforcing female preference to maintain the indirect benefits of choice rather than to reduce the direct costs of coercive mating. We propose a return to a broader view of conflict where indirect selection and intrasexual selection are considered important in the evolution of conflict.

Detecting pigments from colourful eggshells of extinct birds

The known chemical basis of diverse avian eggshell coloration is generated by the same two classes of tetrapyrrole pigments in most living birds. We aimed to extend the evolutionary scope of these patterns by detecting pigments from extinct birds’ eggs. In our samples biliverdin was successfully extracted from subfossil shell fragments of the blue-green egg-laying upland moa Megalapteryx didinus, while protoporphyrin was extracted from the beige eggs of two other extinct moa species. Our data on pigment detection from eggshells of other extant paleognath birds, together with published information on other modern lineages, confirm tetrapyrroles as ubiquitous and conserved pigments contributing to diverse eggshell colours throughout avian evolution.

Sperm storage: distinguishing selective processes and evaluating criteria

Sperm storage, the extended maintenance of viable sperm, probably occurs in most internally fertilizing animals. Because it temporally separates mating from conception, sperm storage can be adaptive in ecologically diverse habitats and affect life histories, mating systems, cryptic female choice, sperm competition, and sexual conflict. Sperm storage can result from different selective forces acting on females and/or males, sometimes resulting in coevolution. The various criteria often used to determine the presence of sperm storage in any given taxon can result from the action of any one or all of these selective forces. Here we discuss the criteria used to study sperm storage and how we can use these to better understand the evolution of diversity in sperm-storage adaptations.

Mechanisms and Evidence of Genital Coevolution: The Roles of Natural Selection, Mate Choice, and Sexual Conflict

Genital coevolution between the sexes is expected to be common because of the direct interaction between male and female genitalia during copulation. Here we review the diverse mechanisms of genital coevolution that include natural selection, female mate choice, male-male competition, and how their interactions generate sexual conflict that can lead to sexually antagonistic coevolution. Natural selection on genital morphology will result in size coevolution to allow for copulation to be mechanically possible, even as other features of genitalia may reflect the action of other mechanisms of selection. Genital coevolution is explicitly predicted by at least three mechanisms of genital evolution: lock and key to prevent hybridization, female choice, and sexual conflict. Although some good examples exist in support of each of these mechanisms, more data on quantitative female genital variation and studies of functional morphology during copulation are needed to understand more general patterns. A combination of different approaches is required to continue to advance our understanding of genital coevolution. Knowledge of the ecology and behavior of the studied species combined with functional morphology, quantitative morphological tools, experimental manipulation, and experimental evolution have been provided in the best-studied species, all of which are invertebrates. Therefore, attention to vertebrates in any of these areas is badly needed.

Sexual conflict over mating in red-sided garter snakes (Thamnophis sirtalis) as indicated by experimental manipulation of genitalia

Sexual conflict over mating can result in sex-specific morphologies and behaviours that allow each sex to exert control over the outcome of reproduction. Genital traits, in particular, are often directly involved in conflict interactions. Via genital manipulation, we experimentally investigated whether genital traits in red-sided garter snakes influence copulation duration and formation of a copulatory plug. The hemipenes of male red-sided garter snakes have a large basal spine that inserts into the female cloaca during mating. We ablated the spine and found that males were still capable of copulation but copulation duration was much shorter and copulatory plugs were smaller than those produced by intact males. We also anaesthetized the female cloacal region and found that anaesthetized females copulated longer than control females, suggesting that female cloacal and vaginal contractions play a role in controlling copulation duration. Both results, combined with known aspects of the breeding biology of red-sided garter snakes, strongly support the idea that sexual conflict is involved in mating interactions in this species. Our results demonstrate the complex interactions among male and female traits generated by coevolutionary processes in a wild population. Such complexity highlights the importance of simultaneous examination of male and female traits.

Evo-devo beyond morphology: from genes to resource use

How does genetic innovation translate into ecological innovation? Although evo-devo has successfully linked genes to morphology, the next stage is elucidating how genes predict resource use. This can be attained by broadening the focus of evo-devo from [genes→morphology], to [genes→morphology→functional ecology]. We suggest that the fields of evo-devo, functional morphology, and evolutionary ecology should be united under a common framework based on three predictions. The first is that morphological disparity should scale positively with functional complexity among different radiations. The second is that functional complexity should correlate negatively with the predictability of evolutionary divergence within lineages, and the third is that functional complexity should define the genetic architecture of adaptive radiations. These predictions could enable a broader understanding of how genetic variation is translated into variation in resource use.

Eggshell conspicuousness in ground nesting birds: do conspicuous eggshells signal nest location to conspecifics?

Predators can adversely impact nesting success and therefore the presence of seemingly conspicuous eggshells would appear maladaptive. The ratites, especially the tinamous, exhibit a diverse array of eggshell colours that appear to differ strikingly from their nesting substrate, while most ground-nesting species that do not build a nest lay camouflaged eggs. Surprisingly, there is little research on how these nest contents appear to ecologically-relevant viewers, including conspecifics and predators. Here we use visual modelling to compare eggshell conspicuousness in two distinct avian lineages differing in eggshell colour and breeding biology: ratites and galliformes. Ratites generally lay vibrant, unspeckled eggs directly on the ground, while galliformes tend to lay subtler, speckled eggs on nests built on the ground. We test the hypothesis that eggshell colours in ratites are more conspicuous, from the perspective of an avian conspecific, than those of galliformes. We found that the uniform colour covering the surface of the eggshell colour (hereafter, eggshell background colour) differs noticeably from the nesting substrate in both ratites and galliformes. However, the speckling pattern of galliform eggs often masks their conspicuous eggshell background colour, which contributes to a less conspicuous appearance overall. We tested the hypothesis that eggshell conspicuousness in ratites serves an intraspecific signalling function to advertise nest location to females in communally nesting species. We found no support for this hypothesis, suggesting that selection pressure for communal laying did not result in the diversity of conspicuousness found in avian eggs. Overall, we argue that future investigations of egg coloration should consider egg appearance (eggshell background colour and speckling) in the context of the natural nest substrate, all from the perspective of the relevant visual receiver.