Sexual dimorphism,phenotypic integration,and the evolution of head structure in casque‐headed lizards

Sexes can differ in features associated with differential reproduction, which can be used during courtship or aggressive encounters. Some traits tend to evolve independently between sexes and emerge as sexually dimorphic within the organismal phenotype. We characterize such a relationship by estimating the phenotypic integration of the head morphology and modularity of the crest in the casque‐headed lizards (Corytophanidae). In this clade, some species show extreme sexual dimorphism (e.g., head crests in the genus Basiliscus) while in others, both sexes are monomorphic. To characterize these patterns, we define phenotypic integration at the interspecific level as a pattern or network of traits evidenced by phylogenetically adjusted correlations that persist among species. At this level, modularity is an increased connectedness (e.g., higher correlation) among sections of these networks that persist in a lineage during the evolution of complex phenotypes. To test both concepts, we used phylogenetic geomorphometrics to characterize the head structure of corytophanid lizards, based on a time‐calibrated phylogeny that includes candidate fossil ancestors. We found evidence of an older diversification of corytophanids than previously reported (~67 vs. ~23.5 MYA) and show that this clade includes two morphological head architectures: (1) Sexually dimorphic crests present in males that are evolving independently from the rest of the head structure, and (2) full integration of the head morphology in monomorphic species. We propose that both architectures are optimal evolutionary trajectories of the parietal crest bones in the head of these lizards. In sexually dimorphic species, these bones are elongated and thinner, and gave rise to the extended crest used in male courtship displays. In monomorphic species, the parietal crest grew thicker in both sexes to allow for a better insertion of muscles associated with a stronger bite.     

Inbreeding depression and genetic load of sexually selected traits: how the guppy lost its spots

To date, few studies have investigated the effects of inbreeding on sexually selected traits, although inbreeding depression on such traits can play an important role in the evolution and ecology of wild populations. Sexually selected traits such as ornamentation and courtship behaviour may not be primary fitness characters, but selection and dominance coefficients of their mutations will resemble those of traits under natural selection. Strong directional selection, for instance, through female mate-choice, purges all but the most recessive deleterious mutations, and the remaining dominance variation will result in inbreeding depression once populations undergo bottlenecks. We analysed the effects of inbreeding on sexually selected traits (colour pattern and courtship behaviour) in the male guppy, Poecilia reticulata, from Trinidad, and found a significant decline in the frequency of mating behaviour and colour spots. Such effects occurred although the genetic basis of these traits, many of which are Y-linked and hemizygous, would be expected to leave relatively little scope for inbreeding depression. Findings suggest that these sexually selected traits could reflect the genetic condition or health of males, and thus may be informative mate-cue characters for female choice as suggested by the 'good genes' model.     

An eye for detail: selective sexual imprinting in zebra finches

To investigate the idea that sexual imprinting creates incipient reproductive isolation between phenotypically diverging populations, I performed experiments to determine whether colony-reared zebra finches would imprint on details of artificial white crests. In the first experiment, adults in one breeding colony wore white crests with a vertical black stripe, while in another colony adults wore crests having a horizontal black stripe; except for their crests, breeders possessed wild-type plumage and conformation. Offspring of both sexes reared in these colonies developed mate preferences for opposite-sexed birds wearing the crest type with which they were reared; neither sex developed a social preference for crested individuals of the same sex. In a second experiment, females reared by crested parents preferred crested males versus males with red leg bands, while control females (reared in a colony of wild-type, uncrested birds) preferred red-banded males in the same test. Results of a third experiment that used sexually dimorphic crest phenotypes indicate that both sexes of offspring imprinted on maternal crest patterns. Results support the hypothesis that sexual imprinting can facilitate isolation both by engendering a preference for population-typical traits and by prioritizing such an imprinting-based preference over species-typical preferences for other traits used in mate choice. Comparison with results of other recent studies indicates that imprinting tendencies of both sexes vary with the characteristics of traits presented as an imprinting stimuli. Tendency to imprint may vary with the perceived information content (e.g., kin, sex, or population indicator) of parental traits, a process dubbed selective sexual imprinting.     

Relationships among male sexually selected traits in the bean bug,Riptortus pedestris (Heteroptera: Alydidae)

Current concepts of sexual selection suggest that male reproductive success is determined by multiple sexual traits. As expression and production of multiple sexual traits are frequently associated with each other, positive or negative correlations among multiple sexual traits ensue. These relationships among traits associated with male reproductive success may be crucial in the evolution of male reproductive strategies. Here, we investigate phenotypic relationships among sexually selected traits in the armed bean bug Riptortus pedestris. In this insect, males with a larger body and weapon are more likely to win male–male competitions, and males with a larger weapon or higher courtship rate are more attractive to females. There was a significant positive correlation between body size and weapon size, whereas the courtship rate had significant negative correlations with body size and weapon size. Our results suggested that there was a phenotypic trade‐off between courtship rate and male morphology. In this insect, smaller males may make more effort in courtship behavior as an alternative mating tactic.     

Experimentally evolved and phenotypically plastic responses to enforced monogamy in a hermaphroditic flatworm

Sexual selection is considered a potent evolutionary force in all sexually reproducing organisms, but direct tests in terms of experimental evolution of sexual traits are still lacking for simultaneously hermaphroditic animals. Here, we tested how evolution under enforced monogamy affected a suite of reproductive traits (including testis area, sex allocation, genital morphology, sperm morphology and mating behaviour) in the outcrossing hermaphroditic flatworm Macrostomum lignano, using an assay that also allowed the assessment of phenotypically plastic responses to group size. The experiment comprised 32 independent selection lines that evolved under either monogamy or polygamy for 20 generations. While we did not observe an evolutionary shift in sex allocation, we detected effects of the selection regime for two male morphological traits. Specifically, worms evolving under enforced monogamy had a distinct shape of the male copulatory organ and produced sperm with shorter appendages. Many traits that did not evolve under enforced monogamy showed phenotypic plasticity in response to group size. Notably, individuals that grew up in larger groups had a more male‐biased sex allocation and produced slightly longer sperm than individuals raised in pairs. We conclude that, in this flatworm, enforced monogamy induced moderate evolutionary but substantial phenotypically plastic responses.     

Evolution of Courtship Behaviour Patterns and Reproductive Isolation in the Desmognathus ochrophaeus Complex

The extent to which differences in courtship behaviour patterns act as mechanisms of reproductive isolation is critical to understanding both speciation and the evolution of these behaviour patterns. While numerous studies have investigated intraspecific and interspecific differences in courtship, fewer interpret results in a phylogenetic framework. We describe and analyse geographic variation in the courtship behaviour patterns of the Allegheny Dusky salamander ( Desmognathus ochrophaeus ). We then examine courtship among closely related species in the D. ochrophaeus complex in a phylogenetic context. We found that populations of D. ochrophaeus separated by extensive geographic distances show little variation in courtship behaviour patterns and are sexually compatible. This contrasts with significant levels of sexual isolation between D. ochrophaeus and other species in the complex. Mapping behaviour patterns onto a phylogeny that we generated from cytochrome b sequences indicates that two behaviour patterns present in the courtship sequence of other members in the complex have either been lost in D. ochrophaeus or gained independently in other species in the complex. Loss of these behaviour patterns may result in reproductive isolation between D. ochrophaeus and its sister taxon, D. orestes .     

The turn of the sword: length increases male swimming costs in swordtails

Sexual selection via female mate choice can result in the evolution of elaborate male traits that incur substantial costs for males. Despite increased interest in how female mating preferences contribute to the evolution of male traits, few studies have directly quantified the locomotor costs of such traits. A sexually selected trait that could affect movement costs is the sword exhibited by male swordtail fishes: while longer swords may increase male mating success, they could negatively affect the hydrodynamic aspects of swimming activities. Here, we examine the energetic costs of the sword in Xiphophorus montezumae by experimentally manipulating sword length and measuring male aerobic metabolism during two types of activity, routine swimming and courtship swimming. Direct measurements of oxygen consumption indicate that males with longer swords expend more energy than males with shortened swords during both types of swimming. In addition, the sword increases the cost of male courtship. Thus, while sexual selection via female choice favours long swords, males with longer swords experience higher metabolic costs during swimming, suggesting that sexual and natural selection have opposing effects on sword evolution. This study demonstrates a hydrodynamic cost of a sexually selected trait. In addition, this study discriminates between the cost of a sexually selected trait used in courtship and other courtship costs.     

Decoupled evolution of display morphology and display behaviour in phrynosomatid lizards

A widespread trend in animals is the evolution of morphological ornaments and behaviours that are involved in aggressive and courtship displays. These display traits are important from the standpoint of communication, sexual selection, and speciation. Previous authors have suggested that the evolution of display morphology and display behaviour should be closely linked. In this study, I tested for this association with behavioural and morphological data for 59 taxa of phrynosomatid lizards using phylogenetic comparative methods (Mad-dison's concentrated changes test and Felsenstein's independent contrasts). The results showed little significant association between features of display morphology and behaviour, suggesting that the evolution of these traits is not tightly coupled. This decoupling is particularly evident in the genus Sceloporus , in which several species have lost the display coloration but retain unmodified display behaviour. The results also suggest that display morphology is more evolutionarily labile than display behaviour in this group.     

Determinants of reproductive success across sequential episodes of sexual selection in a firefly

Because females often mate with multiple males, it is critical to expand our view of sexual selection to encompass pre-, peri- and post-copulatory episodes to understand how selection drives trait evolution. In Photinus fireflies, females preferentially respond to males based on their bioluminescent courtship signals, but previous work has shown that male paternity success is negatively correlated with flash attractiveness. Here, we experimentally manipulated both the attractiveness of the courtship signal visible to female Photinus greeni fireflies before mating and male nuptial gift size to determine how these traits might each influence mate acceptance and paternity share. We also measured pericopulatory behaviours to examine their influence on male reproductive success. Firefly males with larger spermatophores experienced dual benefits in terms of both higher mate acceptance and increased paternity share. We found no effect of courtship signal attractiveness or pericopulatory behaviour on male reproductive success. Taken together with previous results, this suggests a possible trade-off for males between producing an attractive courtship signal and investing in nuptial gifts. By integrating multiple episodes of sexual selection, this study extends our understanding of sexual selection in Photinus fireflies and provides insight into the evolution of male traits in other polyandrous species.     

Patterns of variation in ornaments of Crested Auklets Aethia cristatella

We investigated patterns of variation of feather and bill ornaments of Crested Auklets Aethia cristatella , a monogamous seabird, based on 963 individuals measured in the years 1990 to 1998. Three prominent ornaments were displayed: a forehead crest, composed of 11–31 curved feathers averaging about 40 mm in length, bilaterally symmetrical white auricular plumes on the sides of the head behind the eyes, averaging about 30 mm in length, and brightly coloured semi-circular rictal plates at the corners of the bill. As in other putative sexually selected traits, auklet ornaments were more variable across individuals than non-ornamental traits. Crest length and auricular plume length were positively correlated within individuals but not across years. Among the traits measured there was evidence for slight sexual dimorphism for the auricular plume and rictal plate ornaments and for culmen length and tarsus (males were slightly larger than females) but not for the crest ornament. Breeding adult females and males had greater crest and plume ornament expression than non-breeding adults. Paradoxically, females' crests and rictal plates were more variable than males' crests and rictal plates. Based on independent samples, the expression of feather ornaments and rictal plate varied among years between 1990 and 1998. Crested Auklet ornaments did not vary in concert with the ornaments of Whiskered Aethia pygmaea and Least Auklets Aethia pusilla during this period. Crested Auklet subadults had smaller ornaments than adults. Based on adults remeasured after an interval of one to seven years, the size of individuals' feather ornaments increased with age. We found no relationship between auricular plume length and asymmetry. Male auricular plumes and female crests were weakly correlated with body condition.     

Sexual and natural selection in the evolution of extended phenotypes: the use of green nesting material in starlings

Although sexual selection is typically considered the predominant force driving the evolution of ritualized sexual behaviours, natural selection may also play an important and often underappreciated role. The use of green aromatic plants among nesting birds has been interpreted as a component of extended phenotype that evolved either via natural selection due to potential sanitary functions or via sexual selection as a signal of male attractiveness. Here, we compared both hypotheses using comparative methods in starlings, a group where this behaviour is widespread. We found that the use of green plants was positively related to male‐biased size dimorphism and that it was most likely to occur among cavity‐nesting species. These results suggest that this behaviour is likely favoured by sexual selection, but also related to its sanitary use in response to higher parasite loads in cavities. We speculate that the use of green plants in starlings may be facilitated by cavity nesting and was subsequently co‐opted as a sexual signal by males. Our results represent an example of how an extended phenotypic component of males becomes sexually selected by females. Thus, both natural selection and sexual selection are necessary to fully understand the evolution of ritualized behaviours involved in courtship.     

The Effects of Inbreeding on Male Courtship Behaviour and Coloration in Guppies

Despite an extensive literature on inbreeding depression in a variety of traits, relatively little is known about the effects of inbreeding on patterns of sexual behaviour. In this study, we use the guppy Poecilia reticulata to investigate the influence of parental relatedness (full‐sib. vs. unrelated matings) on sexual behaviour and colour pattern variation in adult male offspring. Our results revealed that one generation of full‐sibling mating resulted in a strong decline in male sexual motivation (courtship intensity and following behaviour) and mating success (number of successful copulations and insemination success – as estimated by the frequency of post‐copulatory jerks after mating), but we detected no significant influence of inbreeding on colour pattern variation. Our finding that sexual ornamentation (colour) did not show similar inbreeding depression to courtship behaviour may be due to differences in the genetic basis of these traits. Our findings indicate that courtship can be a sensitive indicator of genetic stress and add to an emerging picture that sexually selected traits can be severely affected by inbreeding depression.     

Female preference for multi-modal courtship: multiple signals are important for male mating success in peacock spiders

A long-standing goal for biologists has been to understand how female preferences operate in systems where males have evolved numerous sexually selected traits. Jumping spiders of the Maratus genus are exceptionally sexually dimorphic in appearance and signalling behaviour. Presumably, strong sexual selection by females has played an important role in the evolution of complex signals displayed by males of this group; however, this has not yet been demonstrated. In fact, despite apparent widespread examples of sexual selection in nature, empirical evidence is relatively sparse, especially for species employing multiple modalities for intersexual communication. In order to elucidate whether female preference can explain the evolution of multi-modal signalling traits, we ran a series of mating trials using Maratus volans. We used video recordings and laser vibrometry to characterize, quantify and examine which male courtship traits predict various metrics of mating success. We found evidence for strong sexual selection on males in this system, with success contingent upon a combination of visual and vibratory displays. Additionally, independently produced, yet correlated suites of multi-modal male signals are linked to other aspects of female peacock spider behaviour. Lastly, our data provide some support for both the redundant signal and multiple messages hypotheses for the evolution of multi-modal signalling.     

Sex, ecology and the brain: evolutionary correlates of brain structure volumes in Tanganyikan cichlids

Analyses of the macroevolutionary correlates of brain structure volumes allow pinpointing of selective pressures influencing specific structures. Here we use a multiple regression framework, including phylogenetic information, to analyze brain structure evolution in 43 Tanganyikan cichlid species. We analyzed the effect of ecological and sexually selected traits for species averages, the effect of ecological traits for each sex separately and the influence of sexual selection on structure dimorphism. Our results indicate that both ecological and sexually selected traits have influenced brain structure evolution. The patterns observed in males and females generally followed those observed at the species level. Interestingly, our results suggest that strong sexual selection is associated with reduced structure volumes, since all correlations between sexually selected traits and structure volumes were negative and the only statistically significant association between sexual selection and structure dimorphism was also negative. Finally, we previously found that monoparental female care was associated with increased brain size. However, here cerebellum and hypothalamus volumes, after controlling for brain size, associated negatively with female-only care. Thus, in accord with the mosaic model of brain evolution, brain structure volumes may not respond proportionately to changes in brain size. Indeed selection favoring larger brains can simultaneously lead to a reduction in relative structure volumes.     

Multiple male traits interact: attractive bower decorations facilitate attractive behavioural displays in satin bowerbirds

Sexually selected male courtship displays often involve multiple behavioural and physical traits, but little is known about the function of different traits in mate choice. Here, we examine female courtship behaviours to learn how male traits interact to influence female mating decisions. In satin bowerbirds (Ptilonorhynchus violaceus), successful males give highly aggressive, intense behavioural displays without startling females. Males do this by modulating their displays in response to female crouching, which signals the display intensity that females will tolerate without being startled. Females typically visit multiple males for multiple courtships before choosing a mate, and females show differing tolerance for intense displays during their first courtship with each male. We test three hypotheses that may explain this: (i) familiarity with the courting male; (ii) the order of the courtship in mate-searching; and (iii) the attractiveness of the courting male. We found that females are more tolerant of intense displays during first courtships with attractive males; this increased female tolerance may allow attractive males to give higher intensity courtship displays that further enhance their attractiveness. We then examined why this is so, finding evidence that females are less likely to be startled by males with better physical displays (bower decorations), and this reduced startling then contributes to male courtship success. This role of physical displays in facilitating behavioural displays suggests a novel mechanism by which multiple physical and behavioural traits may influence female choice.     

Behavioural mechanisms of sexual isolation involving multiple modalities and their inheritance

Speciation research dissects the genetics and evolution of reproductive barriers between parental species. Hybrids are the “gatekeepers” of gene flow, so it is also important to understand the behavioural mechanisms and genetics of any potential isolation from their parental species. We tested the role of multiple behavioural barriers in reproductive isolation among closely related field crickets and their hybrids (Teleogryllus oceanicus and Teleogryllus commodus). These species hybridize in the laboratory, but the behaviour of hybrids is unusual and there is little evidence for gene flow in the wild. We found that heterospecific pairs exhibited reduced rates of courtship behaviour due to discrimination by both sexes, and that this behavioural isolation was symmetrical. However, hybrids were not sexually selected against and exhibited high rates of courtship behaviour even though hybrid females are sterile. Using reciprocal hybrid crosses, we characterized patterns of interspecific divergence and inheritance in key sexual traits that might underlie the mating patterns we found: calling song, courtship song and cuticular hydrocarbons (CHCs). Song traits exhibited both sex linkage and transgressive segregation, whereas CHCs exhibited only the latter. Calculations of the strength of isolation exerted by these sexual traits suggest that close‐range signals are as important as long‐distance signals in contributing to interspecific sexual isolation. The surprisingly weak mating barriers observed between hybrids and parental species highlight the need to examine reproductive isolating mechanisms and their genetic bases across different potential stages of introgressive hybridization.     

Sexual ornament size and breeding performance in female and male European Shags Phalacrocorax aristotelis

Research into sexual selection and animal ornamentation has been largely directed at males in sexually dimorphic species. In contrast, there is relatively little empirical information on female ornamentation. Using the European Shag Phalacrocorax aristotelis , a species in which both sexes have an ornamental crest during pair formation, we investigated the evidence for (1) a correlation between crest size and breeding performance and (2) assortative pairing on crest size. Crest size appeared unrelated to age in either sex, though our sample of males did not include first-time breeders. The year of study was one in which overall breeding performance at the colony was poor. Females that did not subsequently produce a clutch had significantly smaller crests during the courtship period than those that did, suggesting a link between ornament size and current condition. This relationship was also significant in males. Among those birds that did produce eggs, there was a significant relationship between ornament size and laying date, again significant in both sexes, with early breeders having larger crests. Early breeding is generally associated with relatively high breeding performance in European Shags. Given that both males and females contribute substantially to parental care and that there will be intrasexual differences in quality, choosiness is likely to be favoured in both sexes, and individuals were found to be paired assortatively with respect to crest size. Our results suggest that ornament size is related to state in European Shags, and thus may be involved in mate choice in both sexes.     

Antennal courtship and functional morphology of tyloids in the parasitoid wasp Syrphoctonus tarsatorius (Hymenoptera: Ichneumonidae: Diplazontinae)

Courtship behaviour and associated morphological characters are believed to evolve under diversifying sexual selection. In Hymenoptera, sexually dimorphic antennal structures, the ‘tyloids’, show a large variability. Although crucial for functional interpretation, the link between tyloid morphology and courtship behaviour has gained only limited attention. Here, we investigate antennal morphology and antennal courtship in the parasitoid wasp Syrphoctonus tarsatorius (Hymenoptera: Ichneumonidae: Diplazontinae). We confirm the glandular nature of the tyloids by light and scanning electron microscopy. Moreover, we report a new form of antennation during courtship, antennal double-coiling, which links morphology and behaviour by bringing the tyloids in direct contact with the antennae of the female, thus probably facilitating the transfer of a contact pheromone. We show that a change in haemolymph pressure is the activator of the antennal movement and that it can be reproduced in the laboratory using amputated antennae. Investigations of antennal structure and movement in three additional hymenopteran species suggest that the number and location of tyloids coincide with the modality of antennal coiling. Our method for simulating antennal movement will enable retrieving information about courtship behaviour from museum specimens, thus leading to a better understanding of the evolution of courtship behaviour in Hymenoptera.     

"A taste for the beautiful": latent aesthetic mate preferences for white crests in two species of Australian grassfinches

Darwin first hypothesized that bright colors and elaborate ornamentation of male animals evolved in response to the "aesthetic" mate preferences of females. By this reasoning, potentially costly male secondary sexual traits may evolve not in response to selection for demonstration of vigor but, rather, in response to latent, nonfunctional preferences by females. Recent comparative evidence for this phenomenon is equivocal. Here we present experimental evidence that two avian species from a lineage devoid of crested species have mate preferences for opposite sex conspecifics wearing artificial white crests. Other colors of crests that have been studied are not preferred. Preferences for white crests did not diminish over the longest experimental interval (12 wk). These results are additional powerful evidence for highly structured aesthetic mate preferences in estrildine finches. Sex differences in the expression of preferences, and the widespread occurrence of facial ornamentation in birds, suggest that the preference "structure" is influenced by the central nervous system. We hypothesize that aesthetic preferences are a potent force in the early evolution of sexually selected traits, and that "indicator" traits evolve secondarily from traits initially favored by aesthetic preferences.     

Sexual selection and speciation: Issues raised by Hawaiian Drosophila

The Drosophila fauna of Hawaii is extraordinarily diverse, representing about 25% of the world's described species. The most notable characteristics which differentiate the species in Hawaii are morphological and behavioral ones used in courtship and mating. These flies are excellent model species for investigating the evolution of sexually selected traits. Hypotheses regarding the associations between species formation and mating behaviour have been formulated as a result of work on this group, leading to further empirical and theoretical research.