Climate Change Alters Sexual Signaling in a Desert-Adapted Frog.

AbstractClimate change is altering species' habitats, phenology, and behavior. Although sexual behaviors impact population persistence and fitness, climate change's effects on sexual signals are understudied. Climate change can directly alter temperature-dependent sexual signals, cause changes in body size or condition that affect signal production, or alter the selective landscape of sexual signals. We tested whether temperature-dependent mating calls of Mexican spadefoot toads (Spea multiplicata) had changed in concert with climate in the southwestern United States across 22 years. We document increasing air temperatures, decreasing rainfall, and changing seasonal patterns of temperature and rainfall in the spadefoots' habitat. Despite increasing air temperatures, spadefoots' ephemeral breeding ponds have been getting colder at most elevations, and male calls have been slowing as a result. However, temperature-standardized call characters have become faster, and male condition has increased, possibly due to changes in the selective environment. Thus, climate change might generate rapid, complex changes in sexual signals with important evolutionary consequences.

Females alter their mate preferences depending on hybridization risk.

Mating with another species is often maladaptive because it generally results in no or low-fitness offspring. When hybridization is sufficiently costly, individuals should avoid mating with heterospecifics even if it reduces their ability to mate with high-quality conspecifics that resemble heterospecifics. Here, we used spadefoot toads, Spea multiplicata, to evaluate whether females alter their preferences for conspecific male sexual signals (call rate) depending on heterospecific presence. When presented with conspecific signals against a background including both conspecific and heterospecific signals, females preferred male traits that were most dissimilar to heterospecifics-even though these signals are potentially associated with lower-quality mates. However, when these same females were presented with a background that included only conspecific signals, some females switched their preferences, choosing conspecific signals that were exaggerated and indicative of high-quality conspecific mates. Because only some females switched their preferences between these two chorus treatments, there was no population-level preference for exaggerated conspecific male signals in the absence of heterospecifics. These results show that hybridization risk can alter patterns of mate choice and, consequently, sexual selection on male signals. Moreover, they emphasize that the strength and expression of reproductive barriers between species (such as mate choice) can be context-dependent.

Biased Hybridization and Its Impact on Adaptive Introgression.

Gene exchange between species can influence ecological and evolutionary processes ranging from population rescue to adaptive radiation. Genomic tools have provided new insights into the prevalence and nature of gene exchange between species. However, much remains unknown of how ecological, behavioral, and evolutionary factors determine what genetic variation moves between species in the first place. In particular, more research is needed that evaluates whether such factors bias gene flow from one species to another, and whether any such biases affect how genetic variation from another species is ultimately retained in the genome of a given species. Addressing this issue is crucial in a changing world where hybridization and introgression might determine which species succeed and which become extinct.

Adaptive Plasticity as a Fitness Benefit of Mate Choice.

Phenotypic plasticity and sexual selection can each promote adaptation in variable environments, but their combined influence on adaptive evolution is not well understood. We propose that sexual selection can facilitate adaptation in variable environments when individuals prefer mates that produce adaptively plastic offspring. We develop this hypothesis and review existing studies showing that diverse groups display both sexual selection and plasticity in nonsexual traits. Thus, plasticity could be a widespread but unappreciated benefit of mate choice. We describe methods and opportunities to test this hypothesis and describe how sexual selection might foster the evolution of phenotypic plasticity. Understanding this interplay between sexual selection and phenotypic plasticity might help predict which species will adapt to a rapidly changing world.

Response to Comment on "Females engaging in adaptive hybridization prefer high-quality heterospecifics as mates".

Braun et al contend that we did not account for survival, but we did. Differential survival does not alter our conclusions, which were also robust to removing anomalous families. They ignore the study system's natural history justifying our fitness measures, while failing to account for our behavioral data. We stand by our conclusion that females adaptively choose among heterospecific males.

Character displacement.

David and Karin Pfennig introduce character displacement, the divergent evolution of traits in overlapping species.

Differential encoding of signals and preferences by noradrenaline in the anuran brain.

Social preferences enable animals to selectively interact with some individuals over others. One influential idea for the evolution of social preferences is that preferred signals evolve because they elicit greater neural responses from sensory systems. However, in juvenile plains spadefoot toad (Spea bombifrons), a species with condition-dependent mating preferences, responses of the preoptic area, but not of the auditory midbrain, mirror adult social preferences. To examine whether this separation of signal representation from signal valuation generalizes to other anurans, we compared the relative contributions of noradrenergic signalling in the preoptic area and auditory midbrain of S. bombifrons and its close relative Spea multiplicata We manipulated body condition in juvenile toads by controlling diet and used high pressure liquid chromatography to compare call-induced levels of noradrenaline and its metabolite MHPG in the auditory midbrain and preoptic area of the two species. We found that calls from the two species induced different levels of noradrenaline and MHPG in the auditory system, with higher levels measured in both species for the more energetic S. bombifrons call. In contrast, noradrenaline levels in the preoptic area mirrored patterns of social preferences in both S. bombifrons and S. multiplicata That is, noradrenaline levels were higher in response to the preferred calls within each species and were modified by diet in S. bombifrons (with condition-dependent preferences) but not S. multiplicata (with condition-independent preferences). Our results are consistent with a potentially important role for preoptic noradrenaline in the development of social preferences and indicate that it could be a target of selection in the evolution of condition-dependent social preferences.

Female toads engaging in adaptive hybridization prefer high-quality heterospecifics as mates.

Hybridization-interbreeding between species-is generally thought to occur randomly between members of two species. Contrary to expectation, female plains spadefoot toads (Spea bombifrons) can increase their evolutionary fitness by preferentially mating with high-quality males of another species, the Mexican spadefoot toad (Spea multiplicata). Aspects of Mexican spadefoot males' mating calls predict their hybrid offspring's fitness, and plains spadefoot females prefer Mexican spadefoot males on the basis of these attributes, but only in populations and ecological conditions where hybridization is adaptive. By selecting fitness-enhancing mates of another species, females increase hybridization's benefits and exert sexual selection across species. Nonrandom mating between species can thereby increase the potential for adaptive gene flow between species so that adaptive introgression is not simply happenstance.

Comparing Adaptive Radiations Across Space, Time, and Taxa.

Adaptive radiation plays a fundamental role in our understanding of the evolutionary process. However, the concept has provoked strong and differing opinions concerning its definition and nature among researchers studying a wide diversity of systems. Here, we take a broad view of what constitutes an adaptive radiation, and seek to find commonalities among disparate examples, ranging from plants to invertebrate and vertebrate animals, and remote islands to lakes and continents, to better understand processes shared across adaptive radiations. We surveyed many groups to evaluate factors considered important in a large variety of species radiations. In each of these studies, ecological opportunity of some form is identified as a prerequisite for adaptive radiation. However, evolvability, which can be enhanced by hybridization between distantly related species, may play a role in seeding entire radiations. Within radiations, the processes that lead to speciation depend largely on (1) whether the primary drivers of ecological shifts are (a) external to the membership of the radiation itself (mostly divergent or disruptive ecological selection) or (b) due to competition within the radiation membership (interactions among members) subsequent to reproductive isolation in similar environments, and (2) the extent and timing of admixture. These differences translate into different patterns of species accumulation and subsequent patterns of diversity across an adaptive radiation. Adaptive radiations occur in an extraordinary diversity of different ways, and continue to provide rich data for a better understanding of the diversification of life.

Reinforcement and the Proliferation of Species.

Adaptive radiations are characterized by the rapid proliferation of species. Explaining how adaptive radiations occur therefore depends, in part, on identifying how populations become reproductively isolated-and ultimately become different species. Such reproductive isolation could arise when populations adapting to novel niches experience selection to avoid interbreeding and, consequently, evolve mating traits that minimize such hybridization via the process of reinforcement. Here, we highlight that a downstream consequence of reinforcement is divergence of conspecific populations, and this further divergence can instigate species proliferation. Moreover, we evaluate when reinforcement will-and will not-promote species proliferation. Finally, we discuss empirical approaches to test what role, if any, reinforcement plays in species proliferation and, consequently, in adaptive radiation. To date, reinforcement's downstream effects on species proliferation remain largely unknown and speculative. Because the ecological and evolutionary contexts in which adaptive radiations occur are conducive to reinforcement and its downstream consequences, adaptive radiations provide an ideal framework in which to evaluate reinforcement's role in diversification.

Genome of Spea multiplicata, a Rapidly Developing, Phenotypically Plastic, and Desert-Adapted Spadefoot Toad.

Frogs and toads (anurans) are widely used to study many biological processes. Yet, few anuran genomes have been sequenced, limiting research on these organisms. Here, we produce a draft genome for the Mexican spadefoot toad, Spea multiplicata, which is a member of an unsequenced anuran clade. Atypically for amphibians, spadefoots inhabit deserts. Consequently, they possess many unique adaptations, including rapid growth and development, prolonged dormancy, phenotypic (developmental) plasticity, and adaptive, interspecies hybridization. We assembled and annotated a 1.07 Gb Sp. multiplicata genome containing 19,639 genes. By comparing this sequence to other available anuran genomes, we found gene amplifications in the gene families of nodal, hyas3, and zp3 in spadefoots, and obtained evidence that anuran genome size differences are partially driven by variability in intergenic DNA content. We also used the genome to identify genes experiencing positive selection and to study gene expression levels in spadefoot hybrids relative to their pure-species parents. Completion of the Sp. multiplicata genome advances efforts to determine the genetic bases of spadefoots' unique adaptations and enhances comparative genomic research in anurans.

Variation in hybrid gene expression: Implications for the evolution of genetic incompatibilities in interbreeding species.

Interbreeding species often produce low-fitness hybrids due to genetic incompatibilities between parental genomes. Whether these incompatibilities reflect fixed allelic differences between hybridizing species, or, alternatively, standing variants that segregate within them, remains unknown for many natural systems. Yet, evaluating these alternatives is important for understanding the origins and nature of species boundaries. We examined these alternatives using spadefoot toads (genus Spea), which naturally hybridize. Specifically, we contrasted patterns of gene expression in hybrids relative to pure-species types in experimentally produced tadpoles from allopatric parents versus those from sympatric parents. We evaluated the prediction that segregating variation should result in gene expression differences between hybrids derived from sympatric parents versus hybrids derived from allopatric parents, and found that 24% of the transcriptome showed such differences. Our results further suggest that gene expression in hybrids has evolved in sympatry owing to evolutionary pressures associated with ongoing hybridization. Although we did not measure hybrid incompatibilities directly, we discuss the implications of our findings for understanding the nature of hybrid incompatibilities, how they might vary across populations over time, and the resulting effects on the evolutionary maintenance - or breakdown - of reproductive barriers between species.

Male sexual signal predicts phenotypic plasticity in offspring: implications for the evolution of plasticity and local adaptation.

In a rapidly changing world, understanding the processes that influence a population's ability to respond to natural selection is critical for identifying how to preserve biodiversity. Two such processes are phenotypic plasticity and sexual selection. Whereas plasticity can facilitate local adaptation, sexual selection potentially impedes local adaptation, especially in rapidly changing or variable environments. Here we hypothesize that, when females preferentially choose males that sire plastic offspring, sexual selection can actually facilitate local adaptation to variable or novel environments by promoting the evolution of adaptive plasticity. We tested this hypothesis by evaluating whether male sexual signals could indicate plasticity in their offspring and, concomitantly, their offspring's ability to produce locally adapted phenotypes. Using spadefoot toads ( Spea multiplicata) as our experimental system, we show that a male sexual signal predicts plasticity in his offspring's resource-use morphology. Specifically, faster-calling males (which are preferred by females) produce more plastic offspring; such plasticity, in turn, enables these males' offspring to respond adaptively to the spadefoots' highly variable environment. The association between a preferred male signal and adaptive plasticity in his offspring suggests that female mate choice can favour the evolution and maintenance of phenotypic plasticity and thereby foster adaptation to a variable environment. This article is part of the theme issue 'The role of plasticity in phenotypic adaptation to rapid environmental change'.

Monoaminergic integration of diet and social signals in the brains of juvenile spadefoot toads.

Social behavior often includes the production of species-specific signals (e.g. mating calls or visual displays) that evoke context-dependent behavioral responses from conspecifics. Monoamines are important neuromodulators that have been implicated in context-dependent social behavior, yet we know little about the development of monoaminergic systems and whether they mediate the effects of early life experiences on adult behavior. We examined the effects of diet and social signals on monoamines early in development in the plains spadefoot toad (Spea bombifrons), a species in which diet affects the developmental emergence of species recognition and body condition affects the expression of adult mating preferences. To do so, we manipulated the diet of juveniles for 6 weeks following metamorphosis and collected their brains 40 min following the presentation of either a conspecific or a heterospecific call. We measured levels of monoamines and their metabolites using high pressure liquid chromatography from tissue punches of the auditory midbrain (i.e. torus semicircularis), hypothalamus and preoptic area. We found that call type affected dopamine and noradrenaline signaling in the auditory midbrain and that diet affected dopamine and serotonin in the hypothalamus. In the preoptic area, we detected an interaction between diet and call type, indicating that diet modulates how the preoptic area integrates social information. Our results suggest that the responsiveness of monoamine systems varies across the brain and highlight preoptic dopamine and noradrenaline as candidates for mediating effects of early diet experience on later expression of social preferences.

Genetic variation during range expansion: effects of habitat novelty and hybridization.

How species' ranges evolve remains an enduring problem in ecology and evolutionary biology. Species' range limits are potentially set by the inability of peripheral populations to adapt to range-edge habitat. Indeed, peripheral populations are often assumed to have reduced genetic diversity and population sizes, which limit evolvability. However, support for this assumption is mixed, possibly because the genetic effects of range expansion depend on two factors: the extent that habitat into which expansion occurs is novel and sources of gene flow. Here, we used spadefoot toads, Spea bombifrons, to contrast the population genetic effects of expansion into novel versus non-novel habitat. We further evaluated gene flow from conspecifics and from heterospecifics via hybridization with a resident species. We found that range expansion into novel habitat, relative to non-novel habitat, resulted in higher genetic differentiation, lower conspecific gene flow and bottlenecks. Moreover, we found that hybridizing with a resident species introduced genetic diversity in the novel habitat. Our results suggest the evolution of species' ranges can depend on the extent of differences in habitat between ancestral and newly occupied ranges. Furthermore, our results highlight the potential for hybridization with a resident species to enhance genetic diversity during expansions into novel habitat.

Hybridization as a facilitator of species range expansion.

Explaining the evolution of species geographical ranges is fundamental to understanding how biodiversity is distributed and maintained. The solution to this classic problem in ecology and evolution remains elusive: we still do not fully know how species geographical ranges evolve and what factors fuel range expansions. Resolving this problem is now more crucial than ever with increasing biodiversity loss, global change and movement of species by humans. Here, we describe and evaluate the hypothesis that hybridization between species can contribute to species range expansion. We discuss how such a process can occur and the empirical data that are needed to test this hypothesis. We also examine how species can expand into new environments via hybridization with a resident species, and yet remain distinct species. Generally, hybridization may play an underappreciated role in influencing the evolution of species ranges. Whether-and to what extent-hybridization has such an effect requires further study across more diverse taxa.

Reinforcement as an initiator of population divergence and speciation.

When hybridization results in reduced fitness, natural selection is expected to favor the evolution of traits that minimize the likelihood of hybridizing in the first place. This process, termed reinforcement (or, more generally, reproductive character displacement), thereby contributes to the evolution of enhanced reproductive isolation between hybridizing groups. By enhancing reproductive isolation in this way, reinforcement plays an important role in the final stages of speciation. However, reinforcement can also contribute to the early stages of speciation. Specifically, because selection to avoid hybridization occurs only in sympatric populations, the unfolding of reinforcement can lead to the evolution of traits in sympatric populations that reduce reproduction between conspecifics in sympatry versus those in allopatry. Thus, reinforcement between species can lead to reproductive isolation-and possibly speciation-between populations in sympatry versus those in allopatry or among different sympatric populations. Here, I describe how this process can occur, the conditions under which it is most likely to occur, and the empirical data needed to evaluate the hypothesis that reinforcement can initiate speciation.

Sexual selection's impacts on ecological specialization: an experimental test.

In many species, individuals specialize on different resources, thereby reducing competition. Such ecological specialization can promote the evolution of alternative ecomorphs-distinct phenotypes adapted for particular resources. Elucidating whether and how this process is influenced by sexual selection is crucial for understanding how ecological specialization promotes the evolution of novel traits and, potentially, speciation between ecomorphs. We evaluated the population-level effects of sexual selection (as mediated by mate choice) on ecological specialization in spadefoot toad tadpoles that express alternative ecomorphs. We manipulated whether sexual selection was present or reversed by mating females to their preferred versus non-preferred males, respectively. We then exposed their tadpoles to resource competition in experimental mesocosms. The resulting distribution of ecomorphs was similar between treatments, but sexual selection generated poorer trait integration in, and lower fitness of, the more specialized carnivore morph. Moreover, disruptive and directional natural selection were weaker in the sexual selection present treatment. Nevertheless, this effect on disruptive selection was smaller than previously documented effects of ecological opportunity and competitor density. Thus, sexual selection can inhibit adaptation to resource competition and thereby hinder ecological specialization, particularly when females obtain fitness benefits from mate choice that offset the cost of producing competitively inferior offspring.

Leptin Manipulation Reduces Appetite and Causes a Switch in Mating Preference in the Plains Spadefoot Toad (Spea bombifrons).

Condition- or context-dependent mate choice occurs when females modify their mate preferences depending on their internal or external environment. While the ecological and evolutionary factors that favor the evolution of such plasticity are emerging, relatively little is known of the mechanisms underlying such choice. Here we evaluated whether leptin, a protein hormone involved in the regulation of appetite, might affect the expression of condition-dependent mate choice decisions. To do so, we administered leptin to spadefoot toads, Spea bombifrons, which exhibit condition-dependent mate choice for males of their own species versus congeneric males of S. multiplicata. In particular, poor-condition S. bombifrons are more likely than are good-condition S. bombifrons to prefer S. multiplicata males, but only in environments where hybridization between the two species is beneficial. We found that our leptin treatment reduced appetite in S. bombifrons adults, as was expected from leptin's known effects on appetite. However, although we predicted that leptin would reduce female preferences for heterospecific males, we found the opposite. In particular, our leptin treatment generated a consistent, repeatable preference for heterospecifics in an environment where females generally prefer conspecifics regardless of condition. These results indicate that leptin has the potential to affect female mate choice, but that it might do so in non-intuitive ways.