Evolution of correlated complexity in the radically different courtship signals of birds-of-paradise.
ABSTRACT: Ornaments used in courtship often vary wildly among species, reflecting the evolutionary interplay between mate preference functions and the constraints imposed by natural selection. Consequently, understanding the evolutionary dynamics responsible for ornament diversification has been a longstanding challenge in evolutionary biology. However, comparing radically different ornaments across species, as well as different classes of ornaments within species, is a profound challenge to understanding diversification of sexual signals. Using novel methods and a unique natural history dataset, we explore evolutionary patterns of ornament evolution in a group-the birds-of-paradise-exhibiting dramatic phenotypic diversification widely assumed to be driven by sexual selection. Rather than the tradeoff between ornament types originally envisioned by Darwin and Wallace, we found positive correlations among cross-modal (visual/acoustic) signals indicating functional integration of ornamental traits into a composite unit-the "courtship phenotype." Furthermore, given the broad theoretical and empirical support for the idea that systemic robustness-functional overlap and interdependency-promotes evolutionary innovation, we posit that birds-of-paradise have radiated extensively through ornamental phenotype space as a consequence of the robustness in the courtship phenotype that we document at a phylogenetic scale. We suggest that the degree of robustness in courtship phenotypes among taxa can provide new insights into the relative influence of sexual and natural selection on phenotypic radiations.
Project description:The birds-of-paradise (Aves: Paradisaeidae) are a quintessential example of elaborate ornamental diversification among animals. Ornamental evolution in the birds-of-paradise is exemplified by the presence of a highly integrated courtship phenotype, which is the whole package of plumage ornaments, behaviors and sounds that each species uses during courtship. Characterizing a species' courtship phenotype is therefore a key part of evolutionary and taxonomic investigation in the group. With its unprecedented transmogrification from bird-like form into something abstract and otherworldly, the courtship phenotype of the Superb Bird-of-Paradise, Lophorina superba, is one of the most remarkable of all. Recent research by Irestedt et al. (2017) suggests that the genus Lophorina is not a single species but is likely a complex of three allopatric species spanning the island of New Guinea: L. niedda in the Bird's Head Peninsula of the west, L. superba throughout the central cordillera and L. minor in the Papuan Peninsula of the east. Of these, niedda is the most phenotypically divergent with plumage traits hypothesized to possibly produce differences in ornamental appearance during display. However, the whole courtship phenotype of niedda has not been documented and so the actual extent of differences in ornamental appearance during courtship remain unknown. Here we analyze the first audiovisual recordings of niedda and compare its courtship phenotype with superba to test the hypothesis of potential differences in ornamental appearance. Our main goals are to: (1) provide the first description of the courtship phenotype of niedda in the wild, (2) determine if and how the niedda courtship phenotype differs from superba and (3) evaluate any uncovered differences in light of niedda's newly recognized species status. Our secondary goal is to provide a more thorough characterization of courtship phenotype diversity within the genus Lophorina to facilitate future comparative study within the genus and family. Results show that the niedda courtship phenotype differs substantially from superba in numerous aspects of ornamental appearance, display behavior and sound. We highlight six key differences and conclude that the new species status of niedda is corroborated by the distinctly differentiated ornamental features documented here. With full species status, niedda becomes the fourth endemic bird-of-paradise to the Bird's Head region of Indonesian New Guinea (i.e., the Vogelkop Peninsula), a fact that underscores the importance of this region as a center of endemic biodiversity worthy of enhanced conservation protection.
Project description:Patterns of biodiversity are often explained by ecological processes, where traits that promote novel ways of interacting with the environment (key innovations) play a fundamental role in promoting diversification. However, sexual selection and social competition can also promote diversification through rapid evolution of ornamental traits. Because selection can operate only on existing variation, the tendency of ornamental traits to constrain or enable the production of novel phenotypes is a crucial but often overlooked aspect of diversification. Starlings are a speciose group characterized by diverse iridescent colors produced by nanometer-scale arrays of melanin-containing organelles (melanosomes) that play a central role in sexual selection and social competition. We show that evolutionary lability of these colors is associated with both morphological and lineage diversification in African starlings. The solid rod-like melanosome morphology has evolved in a directional manner into three more optically complex forms that can produce a broader range of colors than the ancestral form, resulting in (i) faster color evolution, (ii) the occupation of novel, previously unreachable regions of colorspace, and ultimately (iii) accelerated lineage diversification. As in adaptive radiations, key innovations in ornament production can provide high phenotypic trait variability, leading to dramatic effects on the tempo and mode of diversification.
Project description:Extravagant male ornaments expressed during reproduction are almost invariably assumed to be sexually selected and evolve through competition for mating opportunities. Yet in species where male reproductive success depends on the defence of offspring, male ornaments could also evolve through social competition for offspring survival. However, in contrast to female ornaments, this possibility has received little attention in males. We show that a male ornament that is traditionally assumed to be sexually selected--the red nuptial coloration of the three-spined stickleback--is under stronger selection for offspring survival than for mating success. Males express most coloration during parenting, when they no longer attract females, and the colour correlates with nest retention and hatching success but not with attractiveness to females. This contradicts earlier assumptions and suggests that social selection for offspring survival rather than for sexual selection for mating success is the main mechanism maintaining the ornament in the population. These results suggest that we should consider other forms of social selection beyond sexual selection when seeking to explain the function and evolution of male ornaments. An incorrect assignment of selection pressures could hamper our understanding of evolution.
Project description:Sex-specific ornaments typically occur in males, but they can also develop in females. While there are several models concerning the evolution of male-specific ornaments, it is not clear how, or under what circumstances, those models apply to female-specific ornament evolution. Here, we present a manipulative field experiment that explores the theoretical 'trait space' of multiple female-specific ornaments to study how these unusual traits evolved. We measured the attractiveness of two female-specific ornaments (pinnate leg scales and inflatable abdominal sacs) in the dance fly Rhamphomyia longicauda in a wild mating swarm. We found significant directional preferences for larger ornaments of both types; however, variation in one of the ornaments (abdominal sacs) was almost three times more effective at improving attractiveness. The abdominal ornament was consistently effective in increasing attractiveness to males regardless of leg ornament expression, while leg ornament size was only effective if abdominal ornaments were very small. These results are consistent with predictions from a sexual conflict model of ornament expression in supporting the probable role of deception in the evolution of female-specific ornaments among dance flies. Sexual conflict can be an important force in generating elaborate sex-specific ornaments in females as well as males.
Project description:The diverse array of phenotypes and courtship displays exhibited by birds-of-paradise have long fascinated scientists and nonscientists alike. Remarkably, almost nothing is known about the genomics of this iconic radiation. There are 41 species in 16 genera currently recognized within the birds-of-paradise family (Paradisaeidae), most of which are endemic to the island of New Guinea. In this study, we sequenced genomes of representatives from all five major clades within this family to characterize genomic changes that may have played a role in the evolution of the group's extensive phenotypic diversity. We found genes important for coloration, morphology, and feather and eye development to be under positive selection. In birds-of-paradise with complex lekking systems and strong sexual dimorphism, the core birds-of-paradise, we found Gene Ontology categories for "startle response" and "olfactory receptor activity" to be enriched among the gene families expanding significantly faster compared to the other birds in our study. Furthermore, we found novel families of retrovirus-like retrotransposons active in all three de novo genomes since the early diversification of the birds-of-paradise group, which might have played a role in the evolution of this fascinating group of birds.
Project description:BACKGROUND: The birds-of-paradise (Paradisaeidae) form one of the most prominent avian examples of sexual selection and show a complex biogeographical distribution. The family has accordingly been used as a case-study in several significant evolutionary and biogeographical syntheses. As a robust phylogeny of the birds-of-paradise has been lacking, these hypotheses have been tentative and difficult to assess. Here we present a well supported species phylogeny with divergence time estimates of the birds-of-paradise. We use this to assess if the rates of the evolution of sexually selected traits and speciation have been excessively high within the birds-of-paradise, as well as to re-interpret biogeographical patterns in the group. RESULTS: The phylogenetic results confirm some traditionally recognized relationships but also suggest novel ones. Furthermore, we find that species pairs are geographically more closely linked than previously assumed. The divergence time estimates suggest that speciation within the birds-of-paradise mainly took place during the Miocene and the Pliocene, and that several polygynous and morphologically homogeneous genera are several million years old. Diversification rates further suggest that the speciation rate within birds-of-paradise is comparable to that of the enitre core Corvoidea. CONCLUSION: The estimated ages of morphologically homogeneous and polygynous genera within the birds-of-paradise suggest that there is no need to postulate a particularly rapid evolution of sexually selected morphological traits. The calculated divergence rates further suggest that the speciation rate in birds-of-paradise has not been excessively high. Thus the idea that sexual selection could generate high speciation rates and rapid changes in sexual ornamentations is not supported by our birds-of-paradise data. Potentially, hybridization and long generation times in polygynous male birds-of-paradise have constrained morphological diversification and speciation, but external ecological factors on New Guinea may also have allowed the birds-of-paradise to develop and maintain magnificent male plumages. We further propose that the restricted but geographically complex distributions of birds-of-paradise species may be a consequence of the promiscuous breeding system.
Project description:Why are there so few small secondary sexual characters? Theoretical models predict that sexual selection should lead to reduction as often as exaggeration, and yet we mainly associate secondary sexual ornaments with exaggerated features such as the peacock's tail. We review the literature on mate choice experiments for evidence of reduced sexual traits. This shows that reduced ornamentation is effectively impossible in certain types of ornamental traits (behavioral, pheromonal, or color-based traits, and morphological ornaments for which the natural selection optimum is no trait), but that there are many examples of morphological traits that would permit reduction. Yet small sexual traits are very rarely seen. We analyze a simple mathematical model of Fisher's runaway process (the null model for sexual selection). Our analysis shows that the imbalance cannot be wholly explained by larger ornaments being less costly than smaller ornaments, nor by preferences for larger ornaments being less costly than preferences for smaller ornaments. Instead, we suggest that asymmetry in signaling efficacy limits runaway to trait exaggeration.
Project description:Sexual selection is proposed to be an important driver of speciation and phenotypic diversification in animal systems. However, previous phylogenetic tests have produced conflicting results, perhaps because they have focused on a single signalling modality (visual ornaments), whereas sexual selection may act on alternative signalling modalities (e.g. acoustic ornaments). Here, we compile phenotypic data from 259 avian sister species pairs to assess the relationship between visible plumage dichromatism-a standard index of sexual selection in birds-and macroevolutionary divergence in the other major avian signalling modality: song. We find evidence for a strong negative relationship between the degree of plumage dichromatism and divergence in song traits, which remains significant even when accounting for other key factors, including habitat type, ecological divergence and interspecific interactions. This negative relationship is opposite to the pattern expected by a straightforward interpretation of the sexual selection-diversification hypothesis, whereby higher levels of dichromatism indicating strong sexual selection should be related to greater levels of mating signal divergence regardless of signalling modality. Our findings imply a 'trade-off' between the elaboration of visual ornaments and the diversification of acoustic mating signals, and suggest that the effects of sexual selection on diversification can only be determined by considering multiple alternative signalling modalities.
Project description:<h4>Background</h4>Females often express the same ornaments as males to a similar or lesser degree. Female ornaments can be adaptive, but little is known regarding their origins and mode of evolution. Current utility does not imply evolutionary causation, and therefore it is possible that female ornamentation evolved due to selection on females, as a correlated response to selection on males (sexual constraint), or a combination of both. We tested these ideas simulating simple models for the evolution of male and female correlated traits, and compared their predictions against the coloration of finches in the genus Carduelis.<h4>Results</h4>For carotenoid-based ornamental coloration, a model of sexual constraint on females fits the Carduelis data well. The two alternative models (sexual constraint on males, and mutual constraint) were rejected as causing the similarities in carotenoid coloration between males and females. For melanin coloration, the correlation between the sexes was weaker, indicating that males and females evolved independently to a greater extent.<h4>Conclusions</h4>This indicates that sexual constraint on females was an important mechanism for the evolution of ornamental carotenoid coloration in females, but less so for melanin coloration. This does not mean that female carotenoid coloration is non-adaptive or maladaptive, because sexual dichromatism could evolve if it were maladaptive. It suggests, however, that most evolution of female carotenoid coloration was male-driven and, when adaptive, may not be an adaptation stricto sensu.
Project description:Males must partition their limited reproductive investments between traits that promote access to females (sexual ornaments and weapons) and traits that enhance fertilization success, such as testes and ejaculates. Recent studies show that if the most weaponized males can monopolize access to females through contest competition, thereby reducing the risk of sperm competition, they tend to invest less in sperm production. However, how males invest in sexual ornaments relative to sperm production remains less clear. If male ornaments serve as badges of status, with high-ranking males attaining near-exclusive access to females, similar to monopolizing females through combat, their expression should also covary negatively with investment in post-mating traits. In a comparative study across primates, which exhibit considerable diversification in sexual ornamentation, male weaponry and testes size, we found relative testes size to decrease with sexual ornaments but increase with canine size. These contrasting evolutionary trajectories might be driven by differential selection, functional constraints or temporal patterns of metabolic investment between the different types of sexual traits. Importantly, however, our results indicate that the theory of relative investments between weapons and testes in the context of monopolizing females can extend to male ornaments.