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Sexual selection and speciation
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Genetics of reproductive traits
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Communication and Cooperation in Bats
Sexual selection and speciation
Does sexual selection cause speciation? This long-standing question is receiving a lot of attention currently, partly because of the special role that mate choice can play in determining gene flow. Sexual selection is thought to cause reproductive isolation when male mating signals and female preferences diversify, because that can lead to sexual isolation among populations. After many years of relative obscurity this question is now in the limelight, and evidence is beginning to accumulate in its support. Yet for the most part, this evidence is limited to inferring a role for sexual selection when mating traits differ between closely related species that avoid mating with each other. We remain remarkably ignorant of how sexual selection causes reproductive isolation. In most systems we lack answers to the fundamental question of what causes mating traits to diverge. Without such divergence in mating traits, sexual selection is unlikely to contribute to reproductive isolation.
Our work tackles this question directly. We take the view that sexual selection is likely to act differently when environments differ, and this different action results in mating trait divergence. We begin by developing a detailed understanding of how ecology affects sexual selection within species of sticklebacks. Then, we compare ecological effects on sexual selection for closely related species that differ ecologically. And finally, we determine how these traits contribute to reproductive isolation. Essentially, our work asks how natural and sexual selection interact to create new species.
We use field and laboratory experiments in a system where both natural (Rundle et al 2000) and sexual selection (Boughman 2001) are implicated in speciation - - species pairs of threespine sticklebacks (Gasterosteus aculeatus complex). This system has multiple populations that differ in ecology and mating traits, and these differences confer reproductive isolation. Experiments focus on nuptial color and body size because these traits isolate all pairs.
Previous work demonstrated that sexual selection is involved in speciation (Boughman 2001). I showed that divergence in male mating signals (nuptial color) and female preference for color contributes to sexual isolation, as predicted by models of sexual selection and speciation. I tested a specific mechanism that could cause divergence in sexual traits ? sensory drive. The sensory drive hypothesis invokes four related processes that cause divergence in mating traits: habitat-specific transmission of male signals, adaptation of female perception to local habitat, perceptual variation contributing to preference variation, and matching of male signals to female perception. I found evidence in support of all four predictions, confirming the importance of sensory drive in trait divergence. Variation in water color (the signaling environment) was correlated to variation in male color, female color perception, and color preference. In addition, the extent of divergence in male signals and female preferences was strongly correlated to the extent of reproductive isolation between populations. This was some of the first evidence that divergent sexual selection contributes to speciation, and is notable because the mechanisms causing sexual isolation were identified. The sensory drive hypothesis predicts that differences in the signaling environment can easily facilitate divergence in mating traits, with reproductive isolation as a result (Boughman 2002). Therefore, this process may contribute importantly to speciation in diverse taxa.
In another project, we ask whether sexual selection acts in arbitrary directions, independent from environment, or is ultimately the product of ecologically-based divergent selection. We investigated the roles of divergent natural and sexual selection in the evolution of sexual isolation between sympatric species of threespine sticklebacks (Boughman, Rundle & Schluter 2005 ). We tested the importance of morphological and behavioral traits in conferring sexual isolation and asked to what extent these traits have diverged in parallel between multiple, independently-evolved species pairs. We used the patterns of evolution in ecological and mating traits to infer the likely nature of selection on sexual isolation. Strong parallel evolution implicates ecologically-based divergent natural and/or sexual selection, whereas arbitrary directionality implicates non-ecological sexual selection or drift. In multiple pairs we found that sexual isolation arises in the same way: assortative mating on body size and asymmetric isolation due to male nuptial color. Body size and color have diverged in a strongly parallel manner similar to ecological traits. Our data implicate ecologically-based divergent natural and sexual selection as engines of speciation in this group.
Divergence in female color preference contributes to premating RI in the species pairs, both because it causes behavioral isolation and because it generates divergent sexual selection on male color. The expression of red color is strongly condition dependent in limnetic males but not in benthic males. Preference strength is correlated with the extent of condition dependence in red color (Boughman 2007). Together with patterns of color expression, these results suggest that sexual selection through female choice acts more strongly on limnetic male color than benthic male color. Moreover, stronger preference within species translates into a greater reliance on color in species recognition (Boughman 2007). Preference evolution therefore generates behavioral isolation because females with strong red preferences are more likely to mate with males expressing high red color and reject males expressing dull or black color. The divergent sexual selection generated by different preferences has contributed to diversification in color.
Genetics of reproductive traits
Our lab is collaborating with Dr. Catherine Peichel, Dr. Brian Fritz, and Tiff Malek at the Hutchinson Cancer Institute on the genetics of color and color perception in sticklebacks. This work is designed to understand the genetics of species differences in traits that confer sexual isolation in sticklebacks. This work is especially exciting as a counterpoint to work on the genetics of speciation in model taxa (e.g., Drosophila) where species are millions of years old and there is extensive intrinsic genetic isolation. The very recent origin of the stickleback species allows us to investigate the genetic changes that occur during the process of speciation. In addition, much work on the genetics of speciation ignores the evolutionary causes of genetic change. Our work starts by identifying those causes and their effect on phenotypes, and then explores the way this shapes the genome.
We explore the genetic basis of these color differences through a combination of quantitative genetics, QTL mapping, and admixture mapping. Our quantitative genetic study indicates that color differences arise through the combined effects of genetics and phenotypic plasticity. Our QTL mapping work finds several QTL of moderate effect on three chromosomes, but no sex linkage. We also have evidence suggesting that color and color perception may be genetically linked. Such linkage would facilitate the coevolution of color and color preference, and may help to explain their rapid divergent evolution. In our admixture mapping we are using the hybridizing pair in Enos Lake, where interbreeding for about 10 generations has produced many fish with intermediate color. A preliminary genome scan uncovers at least one region of the genome underlying the difference in male nuptial color in this natural hybrid population. Currently we are increasing marker density and sample size to improve power and resolution to verify this result and find other regions contributing to color difference. Our eventual aim is twofold: to find the genes responsible for color differences, and explore how selection has acted on those genes.
Communication and Cooperation in Bats
Animals that live in stable social groups often cooperate to find and defend limiting resources, such as food or sites for reproduction. When social groups also control access to these limiting resources, membership in a social group can be an essential component of individual fitness. Indicating group membership and discriminating group mates from others should be favored under such circumstances. Signals that indicate group membership are shaped by the function they serve; they should vary among social groups at the individual or group level, and individuals should be able to discriminate between signals given by group mates and others. To retain reliability, group membership signals should also be difficult or costly for outsiders to imitate.
Female greater spear-nosed bats, Phyllostomus hastatus, use audible frequency calls, termed screech calls, to coordinate foraging among long term associates. Field observations imply that females use screech calls to identify members of their social group who not only live but forage together (Wilkinson & Boughman 1998). We showed that females benefit from group foraging by improved food finding and better defense of rich resources. Benefits are limited to females who forage with social group mates (Wilkinson & Boughman 1999). Our work shows that group signatures are an important mechanism to facilitate cooperation among these unrelated females. Partly because of the difficulty in gathering data, bats are a woefully understudied taxon. Thus, this is one of the first studies that determined call function in a natural population. It is especially interesting because of the insights it gave us into this species’ social and cooperative behavior, and how they communicate.
My dissertation work determined call function more precisely and showed that screech calls are group signatures. I characterized the acoustic structure of screech calls recorded in the field and lab, and tested which aspects of identity are encoded in calls. Results demonstrated that screech calls are structured to convey the group membership of the caller, but not individual identity (Boughman 1997). I also found that calls differ between cave colonies. I used field and lab playback experiments to test call function, and found that bats can detect colony and group differences but do not differentiate among individuals based on screech calls (Boughman & Wilkinson 1998). These results were surprising because of the ubiquity of individually distinct vocalizations. This implies that, within the context of cooperative foraging, group membership is essential and individual identity less crucial. Combined with results on the composition of foraging groups, these results indicate that group foraging is mutualistic, and argue against alternative explanations such as reciprocal altruism.
The members of social groups cooperate in foraging and give calls very similar to one another, yet these females are not closely related. Thus, kin selection is unlikely to explain cooperative foraging and vocal similarity does not arise from genetic similarity. To test the hypothesis that vocal convergence is due to vocal learning, I transferred bats reciprocally between social groups. Transfers and residents showed dramatic convergence in call structure. This experiment provided strong evidence that group differences arise through vocal learning. Comparisons of transfers with age-matched half-sibs indicated that call changes are not simply due to maturation, the physical environment, or heredity. Social modification of calls allows females to adjust their calls when social group composition changes. Call modification is not immediate, and the time required for individuals to match a new group could provide protection against outsiders who might feign identity to obtain access to resources controlled by social groups. This work provides important and rare experimental evidence of vocal learning in a mammal (Boughman 1998). It suggests that we should expect vocal learning when call similarity is essential for call function (Boughman & Moss 2003). Future work will test hypotheses developed in this review on the factors that favor vocal learning in mammals.
In a collaborative project, we followed up on these results by investigating auditory perception, and matching of perception and call structure (Bohn, Boughman, Wilkinson & Moss, 2004). We found close matching between auditory sensitivity and frequency of social calls that facilitate mother-pup interactions. We did not find close matching between sensitivity and screech calls. Future work will continue to explore the interaction between perception, communication, and social behavior in this and other bat species. Primary questions to be addressed revolve around understanding selective forces shaping communication signals, and how communication mediates cooperation and conflict.
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