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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.
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Anuros , Cambio Climático , Animales , Masculino , Adaptación Fisiológica , Reproducción , EcosistemaRESUMEN
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.
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Preferencia en el Apareamiento Animal , Humanos , Animales , Masculino , Femenino , Hibridación Genética , Anuros/genética , Reproducción , Conducta Sexual AnimalRESUMEN
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.
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Anuros , Norepinefrina , Animales , Bufonidae , Área Preóptica , ReproducciónRESUMEN
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.
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Especiación Genética , Hibridación Genética , Selección Genética , Adaptación Biológica , Animales , Ecosistema , Aislamiento Reproductivo , Conducta Sexual AnimalRESUMEN
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.
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Adaptación Biológica , Especiación Genética , Animales , Filogeografía , Plantas , Análisis Espacial , TiempoRESUMEN
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.
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Anuros/clasificación , Anuros/genética , Quimera/genética , Regulación del Desarrollo de la Expresión Génica/genética , Hibridación Genética/genética , Animales , Quimera/fisiología , Expresión Génica/genética , Larva/metabolismo , Transcriptoma/genéticaRESUMEN
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.
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Anuros/genética , Ecosistema , Variación Genética , Genética de Población , Hibridación Genética , Animales , Flujo GénicoRESUMEN
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 40â 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.
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Comunicación Animal , Anuros/crecimiento & desarrollo , Anuros/metabolismo , Monoaminas Biogénicas/metabolismo , Dieta , Animales , Femenino , Hipotálamo/metabolismo , Masculino , Mesencéfalo/metabolismo , Área Preóptica/metabolismoRESUMEN
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.
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Distribución Animal , Evolución Biológica , Hibridación Genética , Dispersión de las Plantas , AnimalesRESUMEN
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.
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Anuros/fisiología , Preferencia en el Apareamiento Animal , Adaptación Fisiológica , Animales , Anuros/anatomía & histología , Ecosistema , Conducta Alimentaria , Femenino , Larva/anatomía & histología , Larva/fisiología , Masculino , Fenotipo , Selección GenéticaRESUMEN
Reproductive character displacement is the adaptive evolution of traits that minimize deleterious reproductive interactions between species. When arising from selection to avoid hybridization, this process is referred to as reinforcement. Reproductive character displacement generates divergence not only between interacting species, but also between conspecific populations that are sympatric with heterospecifics versus those that are allopatric. Consequently, such conspecific populations can become reproductively isolated. We compared female mate preferences in, and evaluated gene flow between, neighbouring populations of spadefoot toads that did and did not occur with heterospecifics (mixed- and pure-species populations, respectively). We found that in mixed-species populations females significantly preferred conspecifics. Such females also tended to prefer a conspecific call character that was dissimilar from heterospecifics. By contrast, females from pure-species populations did not discriminate conspecific from heterospecific calls. They also preferred a more exaggerated conspecific call character that resembles heterospecific males. Moreover, gene flow was significantly reduced between mixed- and pure-species population types. Thus, character displacement (and, more specifically, reinforcement) may initiate reproductive isolation between conspecific populations that differ in interactions with heterospecifics.
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Anuros/fisiología , Aislamiento Reproductivo , Conducta Sexual Animal , Animales , Femenino , Flujo Génico , Genética de Población , Masculino , Preferencia en el Apareamiento Animal , Refuerzo en PsicologíaRESUMEN
Amphibians represent a diverse group of tetrapods, marked by deep divergence times between their three systematic orders and families. Studying amphibian biology through the genomics lens increases our understanding of the features of this animal class and that of other terrestrial vertebrates. The need for amphibian genomics resources is more urgent than ever due to the increasing threats to this group. Amphibians are one of the most imperiled taxonomic groups, with approximately 41% of species threatened with extinction due to habitat loss, changes in land use patterns, disease, climate change, and their synergistic effects. Amphibian genomics resources have provided a better understanding of ontogenetic diversity, tissue regeneration, diverse life history and reproductive modes, antipredator strategies, and resilience and adaptive responses. They also serve as critical models for understanding widespread genomic characteristics, including evolutionary genome expansions and contractions given they have the largest range in genome sizes of any animal taxon and multiple mechanisms of genetic sex determination. Despite these features, genome sequencing of amphibians has significantly lagged behind that of other vertebrates, primarily due to the challenges of assembling their large, repeat-rich genomes and the relative lack of societal support. The advent of long-read sequencing technologies, along with computational techniques that enhance scaffolding capabilities and streamline computational workload is now enabling the ability to overcome some of these challenges. To promote and accelerate the production and use of amphibian genomics research through international coordination and collaboration, we launched the Amphibian Genomics Consortium (AGC) in early 2023. This burgeoning community already has more than 282 members from 41 countries (6 in Africa, 131 in the Americas, 27 in Asia, 29 in Australasia, and 89 in Europe). The AGC aims to leverage the diverse capabilities of its members to advance genomic resources for amphibians and bridge the implementation gap between biologists, bioinformaticians, and conservation practitioners. Here we evaluate the state of the field of amphibian genomics, highlight previous studies, present challenges to overcome, and outline how the AGC can enable amphibian genomics research to "leap" to the next level.
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Hybrid male sterility is a common reproductive isolating barrier between species. Yet, little is known about the actual developmental causes of this phenomenon, especially in naturally hybridizing species. We sought to evaluate the developmental causes of hybrid male sterility, using spadefoot toads as our study system. Plains spadefoot toads (Spea bombifrons) and Mexican spadefoot toads (S. multiplicata) hybridize where they co-occur in the southwestern USA. Hybrids are viable, but hybrid males suffer reduced fertility. We compared testes size and developmental stages of sperm cell maturation between hybrid males and males of each species. We found that testes of hybrid males did not differ in mean size from pure-species males. However, hybrids showed a greater range of within-individual variation in testes size than pure-species males. Moreover, although hybrids produced similar numbers of early stage sperm cells, hybrids produced significantly fewer mature spermatozoids than pure-species males. Interestingly, an introgressed individual produced numbers of live sperm comparable to pure-species males, but the majority of these sperm cells were abnormally shaped and non-motile. These results indicate that hybrid incompatibilities in late sperm development serve as a reproductive isolating barrier between species. The nature of this breakdown highlights the possibilities that hybrid males may vary in fertility and that fertility could possibly be recovered in introgressed males.
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Anuros/clasificación , Anuros/fisiología , Hibridación Genética , Espermatogénesis , Animales , Anuros/anatomía & histología , Anuros/genética , Especiación Genética , Infertilidad Masculina/veterinaria , Masculino , Espermatozoides/citología , Espermatozoides/fisiología , Testículo/anatomía & histología , Testículo/fisiologíaRESUMEN
Monoamines are important neuromodulators that respond to social cues and that can, in turn, modify social responses. Yet we know very little about the ontogeny of monoaminergic systems and whether they contribute to the development of social behavior. Anurans are an excellent model for studying the development of social behavior because one of its primary components, phonotaxis, is expressed early in life. To examine the effect of social signals on monoamines early in ontogeny, we presented juvenile Mexican spadefoot toads (Spea multiplicata) with a male mating call or no sound and measured norepinephrine, epinephrine, dopamine, serotonin, and a serotonin metabolite, across the brain using high-pressure liquid chromatography. Our results demonstrate that adult-like monoaminergic systems are in place shortly after metamorphosis. Perhaps more interestingly, we found that mating calls increased the level of monoamines in the juvenile tegmentum, a midbrain region involved in sensory-motor integration and that contributes to brain arousal and attention. We saw no such increase in the auditory midbrain or in forebrain regions. We suggest that changes in monoamine levels in the juvenile tegmentum may reflect the effects of social signals on arousal state and could contribute to context-dependent modulation of social behavior.
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Anuros/metabolismo , Dopamina/metabolismo , Mesencéfalo/metabolismo , Serotonina/metabolismo , Conducta Social , Envejecimiento , Animales , Conducta Animal/fisiología , Cromatografía Líquida de Alta PresiónRESUMEN
Whether environmental effects during juvenile development can alter the ontogeny of adult mating behaviour remains largely unexplored. We evaluated the effect of diet on the early expression of conspecific recognition in spadefoot toads, Spea bombifrons. We found that juvenile toads display phonotaxis behaviour six weeks post-metamorphosis. However, preference for conspecifics versus heterospecifics emerged later and was diet dependent. Thus, the environment can affect the early development of species recognition in a way that might alter adult behaviour. Evaluating such effects is important for understanding variation in hybridization between species and the nature of species boundaries.
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Anuros/fisiología , Dieta , Reconocimiento en Psicología/fisiología , Conducta Sexual Animal/fisiología , Estimulación Acústica , Factores de Edad , Animales , Arizona , Evolución Biológica , Pesos y Medidas Corporales , Hibridación Genética , Actividad Motora/fisiología , Especificidad de la EspecieRESUMEN
Reproductive character displacement--the evolution of traits that minimize reproductive interactions between species--can promote striking divergence in male signals or female mate preferences between populations that do and do not occur with heterospecifics. However, reproductive character displacement can affect other aspects of mating behaviour. Indeed, avoidance of heterospecific interactions might contribute to spatial (or temporal) aggregation of conspecifics. We examined this possibility in two species of hybridizing spadefoot toad (genus Spea). We found that in Spea bombifrons sympatric males were more likely than allopatric males to associate with calling males. Moreover, contrary to allopatric males, sympatric S. bombifrons males preferentially associated with conspecific male calls. By contrast, Spea multiplicata showed no differences between sympatry and allopatry in likelihood to associate with calling males. Further, sympatric and allopatric males did not differ in preference for conspecifics. However, allopatric S. multiplicata were more variable than sympatric males in their responses. Thus, in S. multiplicata, character displacement may have refined pre-existing aggregation behaviour. Our results suggest that heterospecific interactions can foster aggregative behaviour that might ultimately contribute to clustering of conspecifics. Such clustering can generate spatial or temporal segregation of reproductive activities among species and ultimately promote reproductive isolation.
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Adaptación Biológica/fisiología , Anuros/fisiología , Evolución Biológica , Reproducción/fisiología , Conducta Sexual Animal/fisiología , Conducta Social , Estimulación Acústica , Animales , Femenino , Masculino , Reproducción/genética , Sudoeste de Estados Unidos , Especificidad de la EspecieRESUMEN
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.
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Flujo Génico , Hibridación Genética , Evolución Biológica , Genoma , GenómicaRESUMEN
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.
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Adaptación Fisiológica , Reproducción , Aclimatación , Adaptación Fisiológica/genética , Evolución Biológica , Humanos , FenotipoRESUMEN
In The Origin of Species, Darwin proposed his principle of divergence of character (a process now termed "character displacement") to explain how new species arise and why they differ from each other phenotypically. Darwin maintained that the origin of species and the evolution of differences between them is ultimately caused by divergent selection acting to minimize competitive interactions between initially similar individuals, populations, and species. Here, we examine the empirical support for the various claims that constitute Darwin's principle, specifically that (1) competition promotes divergent trait evolution, (2) the strength of competitively mediated divergent selection increases with increasing phenotypic similarity between competitors, (3) divergence can occur within species, and (4) competitively mediated divergence can trigger speciation. We also explore aspects that Darwin failed to consider. In particular, we describe how (1) divergence can arise from selection acting to lessen reproductive interactions, (2) divergence is fueled by the intersection of character displacement and sexual selection, and (3) phenotypic plasticity may play a key role in promoting character displacement. Generally, character displacement is well supported empirically, and it remains a vital explanation for how new species arise and diversify.
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Evolución Biológica , Especiación Genética , Adaptación Fisiológica/genética , Animales , Biología/historia , Ecosistema , Historia del Siglo XIX , Historia del Siglo XX , Historia del Siglo XXI , Fenotipo , Selección Genética , Factores de TiempoRESUMEN
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.