J. Albert C. Uy

Vertebrate pigmentation: from underlying genes to adaptive function

Animal coloration is a powerful model for studying the genetic mechanisms that determine phenotype. Genetic crosses of laboratory mice have provided extensive information about the patterns of inheritance and pleiotropic effects of loci involved in pigmentation. Recently, the study of pigmentation genes and their functions has extended into wild populations, providing additional evidence that pigment gene function is largely conserved across disparate vertebrate taxa and can influence adaptive coloration, often in predictable ways. These new and integrative studies, along with those using a genetic approach to understand color perception, raise some important questions. Most notably, how does selection shape both phenotypic and genetic variation, and how can we use this information to further understand the phenotypic diversity generated by evolutionary processes?

Plumage and song differences mediate species recognition between incipient flycatcher species of the Solomon Islands

Changes in mating signals among populations contribute to species formation. Often these signals involve a suite of display traits of different sensory modalities (“multimodal signals”); however, few studies have tested the consequences of multimodal signal divergence with most focusing on only a single divergent signal or suite of signals of the same sensory modality. Populations of the chestnut-bellied flycatcher Monarcha castaneiventris vary in song and plumage color across the Solomon Islands. Using taxidermic mount presentation and song playback experiments, we tested for the relative roles of divergent song and color in homotypic (“same type”) recognition between one pair of recently diverged sister taxa (the nominate chestnut-bellied M. c. castaneiventris and the white-capped M. c. richardsii forms). We found that both plumage and song type influenced the intensity of aggressive response by territory-owners, with plumage color playing a stronger role. These results indicate that differences in plumage and song are used in homotypic recognition, suggesting the importance of multimodal signal divergence in the evolution of premating reproductive isolation.

Sexual selection accelerates signal evolution during speciation in birds

Sexual selection is proposed to be an important driver of diversification in animal systems, yet previous tests of this hypothesis have produced mixed results and the mechanisms involved remain unclear. Here, we use a novel phylogenetic approach to assess the influence of sexual selection on patterns of evolutionary change during 84 recent speciation events across 23 passerine bird families. We show that elevated levels of sexual selection are associated with more rapid phenotypic divergence between related lineages, and that this effect is restricted to male plumage traits proposed to function in mate choice and species recognition. Conversely, we found no evidence that sexual selection promoted divergence in female plumage traits, or in male traits related to foraging and locomotion. These results provide strong evidence that female choice and male–male competition are dominant mechanisms driving divergence during speciation in birds, potentially linking sexual selection to the accelerated evolution of pre-mating reproductive isolation.

Difference in plumage color used in species recognition between incipient species is linked to a single amino acid substitution in the melanocortin-1 receptor.

Many studies demonstrate that differences in mating signals are used by incipient species in recognizing potential mates or sexual competitors (i.e., species recognition). Little is known, however, about the genetic changes responsible for these differences in mating signals. Populations of the Monarcha castaneiventris flycatcher vary in plumage color across the Solomon Islands, with a subspecies on Makira Island having chestnut bellies and blue‐black upper parts (Monarcha castaneiventris megarhynchus) and a subspecies on neighboring satellite islands being entirely blue‐black (melanic; Monarcha castaneiventris ugiensis). Here we show that a single nonsynonymous point mutation in the melanocortin‐1 receptor (MC1R) gene is present in all melanic birds from one island (Santa Ana) but absent in all chestnut‐bellied birds from Makira Island, implicating this mutation in causing melanism. Birds from a second satellite island (Ugi) do not show the same perfect association between this MC1R variant and plumage color, suggesting an alternative mechanism for melanism on this island. Finally, taxidermic mount presentation experiments in Makira (chestnut) and Santa Ana (melanic) suggest that the plumage difference mediates species recognition. Assuming that the signals used in species recognition are also used in mutual mate choice, our results indicate that a single amino acid substitution contributes to speciation.

Variation in the temporal and spatial use of signals and its implications for multimodal communication

The use of signals across multiple sensory modalities in communication is common in animals and plants. Determining the information that each signal component conveys has provided unique insights into why multimodal signals evolve. However, how these complex signals are assessed by receivers will also influence their evolution, a hypothesis that has received less attention. Here, we explore multimodal signal assessment in a closely related complex of island flycatchers that have diverged in visual and acoustic signals. Using field experiments that manipulated song and plumage colour, we tested if song, a possible long-range signal, is assessed before plumage colour in conspecific recognition. We find that divergent song and colour are assessed in sequence, and this pattern of sequential assessment is likely mediated by habitat structure and the extent of differences in signal characteristics. A broad survey of the literature suggests that many organisms from a wide range of taxa sequentially assess multimodal signals, with long-range signals attracting conspecifics for further assessment of close-range signals. Our results highlight the need to consider how signals are assessed when understanding multimodal signal evolution. Finally, given the results of our field experiments indicating sequential assessment of divergent song and colour in the recognition of conspecifics, we discuss the consequences of multimodal signal divergence for the origin of species, as changes in signals across different sensory modalities may influence the evolution of premating reproductive isolation.

Genomic approaches to understanding population divergence and speciation in birds

ABSTRACT The widespread application of high-throughput sequencing in studying evolutionary processes and patterns of diversification has led to many important discoveries. However, the barriers to utilizing these technologies and interpreting the resulting data can be daunting for first-time users. We provide an overview and a brief primer of relevant methods (e.g., whole-genome sequencing, reduced-representation sequencing, sequence-capture methods, and RNA sequencing), as well as important steps in the analysis pipelines (e.g., loci clustering, variant calling, whole-genome and transcriptome assembly). We also review a number of applications in which researchers have used these technologies to address questions related to avian systems. We highlight how genomic tools are advancing research by discussing their contributions to 3 important facets of avian evolutionary history. We focus on (1) general inferences about biogeography and biogeographic history, (2) patterns of gene flow and isolation upon secondary contact and hybridization, and (3) quantifying levels of genomic divergence between closely related taxa. We find that in many cases, high-throughput sequencing data confirms previous work from traditional molecular markers, although there are examples in which genome-wide genetic markers provide a different biological interpretation. We also discuss how these new data allow researchers to address entirely novel questions, and conclude by outlining a number of intellectual and methodological challenges as the genomics era moves forward.

BEHAVIORAL PATERNITY PREDICTS GENETIC PATERNITY IN SATIN BOWERBIRDS (PTILONORHYNCHUS VIOLACEUS), A SPECIES WITH A NON-RESOURCE-BASED MATING SYSTEM

Abstract The potential for differences between genetic paternity and paternity inferred from behavioral observation has long been recognized. These differences are associated with the challenge for females of seeking both genetic and material benefits; this challenge is less severe in species with polygynous, non-resource-based mating systems (such as leks) than in those with resource-based systems. We present the first study of paternity patterns in a non-resource-based species that does not form true leks. We compared paternity inferred from observed mating behavior to genetically assigned paternity in the Satin Bowerbird (Ptilonorhynchus violaceus) using eight microsatellite markers. Mating behavior was observed and recorded via automated video-cameras positioned at all bowers (29–34 bowers each year) in the study site throughout each mating season. We obtained blood samples and identified mothers for 11 chicks in 9 nests. For all chicks, the most likely genetic father had been observed to mate with the mother in the year the chick was sampled. All most likely genetic fathers were assigned with high confidence and all were bower-holding males. These results demonstrate that genetic paternity can be inferred from observed mating behavior with reasonable confidence in Satin Bowerbirds. Observed male mating-success is therefore a reliable predictor of reproductive success, and this suggests that high skew in observed male mating-success translates directly to high skew in reproductive success. La Paternidad Comportamental Predice la Paternidad Genética en Ptilonorhynchus violaceus, una Especie con un Sistema de Apareamiento que No Está Basado en los Recursos

Alternative mating strategies may favour the persistence of a genetically based colour polymorphism in a pentamorphic fish

Males of the pentamorphic fish, Poecilia parae, show a striking colour polymorphism that ranges from drab coloration resembling females to brilliant black and red stripes. We tested the hypothesis that the observed polymorphism may persist because each morph uses a unique but equally successful mating strategy. We quantified the mating behaviour, testes investment and sperm morphometrics of each morph. We found that the smallest morph (immaculata), which resembles drab females, used a ‘sneaker’ tactic (i.e. forgoing courtship and mostly ‘stealing’ copulations) as a mating strategy. Immaculata males also had larger testes, and produced larger ejaculates and sperm with longer flagella, which should provide advantages during sperm competition. The largest morph (parae) and the coloured blue, red and yellow morphs used a combination of courtship and sneaker tactics. However, they achieved greater copulation success as a result of courtships. The testes investment of parae and yellow morphs were similar but larger than those of the blue and red males. Our results suggest that male morphs of the pentamorphic Poecilia parae use unique mating strategies that exploit different aspects of pre- and postcopulatory sexual selection, which, in turn, may help maintain their relatively stable frequencies in the wild.

Intrasexual competition facilitates the evolution of alternative mating strategies in a colour polymorphic fish

BackgroundIntense competition for access to females can lead to males exploiting different components of sexual selection, and result in the evolution of alternative mating strategies (AMSs). Males of Poecilia parae, a colour polymorphic fish, exhibit five distinct phenotypes: drab-coloured (immaculata), striped (parae), structural-coloured (blue) and carotenoid-based red and yellow morphs. Previous work indicates that immaculata males employ a sneaker strategy, whereas the red and yellow morphs exploit female preferences for carotenoid-based colours. Mating strategies favouring the maintenance of the other morphs remain to be determined. Here, we report the role of agonistic male-male interactions in influencing female mating preferences and male mating success, and in facilitating the evolution of AMSs.ResultsOur study reveals variation in aggressiveness among P. parae morphs during indirect and direct interactions with sexually receptive females. Two morphs, parae and yellow, use aggression to enhance their mating success (i.e., number of copulations) by 1) directly monopolizing access to females, and 2) modifying female preferences after winning agonistic encounters. Conversely, we found that the success of the drab-coloured immaculata morph, which specializes in a sneak copulation strategy, relies in its ability to circumvent both male aggression and female choice when facing all but yellow males.ConclusionsStrong directional selection is expected to deplete genetic variation, yet many species show striking genetically-based polymorphisms. Most studies evoke frequency dependent selection to explain the persistence of such variation. Consistent with a growing body of evidence, our findings suggest that a complex form of balancing selection may alternatively explain the evolution and maintenance of AMSs in a colour polymorphic fish. In particular, this study demonstrates that intrasexual competition results in phenotypically distinct males exhibiting clear differences in their levels of aggression to exclude potential sexual rivals. By being dominant, the more aggressive males are able to circumvent female mating preferences for attractive males, whereas another male type incorporates subordinate behaviours that allow them to circumvent male aggression and female mating preferences. Together, these and previous results indicate that exploiting different aspects of social interactions may allow males to evolve distinct mating strategies and thus the long term maintenance of polymorphisms within populations.

Size-dependent alternative male mating tactics in the yellow dung fly, Scathophaga stercoraria

Whenever males can monopolize females and/or resources used by females, the opportunity for sexual selection will be great. The greater the variation among males in reproductive success, the greater the intensity of selection on less competitive males to gain matings through alternative tactics. In the yellow dung fly, Scathophaga stercoraria, males aggressively compete for access to receptive, gravid females on fresh dung. Larger males are better able to acquire mates and to complete copulation successfully and guard the female throughout oviposition. Here we demonstrate that when an alternative resource is present where females aggregate (i.e. apple pomace, where both sexes come to feed), smaller males will redirect their searching for females from dung to the new substrate. In addition, we identify a class of particularly small males on the alternative substrate that appears never to be present searching for females on or around dung. Smaller males were found to have a mating ‘advantage’ on pomace, in striking contrast to the pattern observed on dung, providing further support for the existence of an alternative male reproductive tactic in this species.