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A new evolutionary model of mate choice copying, published in PLOS Biology, aims to reconcile mismatches between theory and data by proposing that juvenile females mistakenly imprint on male phenotypes that were not in fact preferred by the female they copied.
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Evolução Biológica , Seleção Sexual , Masculino , Humanos , Feminino , FenótipoRESUMO
Generations of scientists have pursued the goal of defining beauty. While early scientists initially focused on objective criteria of beauty ('feature-based aesthetics'), philosophers and artists alike have since proposed that beauty arises from the interaction between the object and the individual who perceives it. The aesthetic theory of fluency formalizes this idea of interaction by proposing that beauty is determined by the efficiency of information processing in the perceiver's brain ('processing-based aesthetics'), and that efficient processing induces a positive aesthetic experience. The theory is supported by numerous psychological results, however, to date there is no quantitative predictive model to test it on a large scale. In this work, we propose to leverage the capacity of deep convolutional neural networks (DCNN) to model the processing of information in the brain by studying the link between beauty and neuronal sparsity, a measure of information processing efficiency. Whether analyzing pictures of faces, figurative or abstract art paintings, neuronal sparsity explains up to 28% of variance in beauty scores, and up to 47% when combined with a feature-based metric. However, we also found that sparsity is either positively or negatively correlated with beauty across the multiple layers of the DCNN. Our quantitative model stresses the importance of considering how information is processed, in addition to the content of that information, when predicting beauty, but also suggests an unexpectedly complex relationship between fluency and beauty.
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Arte , Julgamento , Julgamento/fisiologia , Cognição , Estética , Redes Neurais de ComputaçãoRESUMO
Communication signals often comprise an array of colours, lines, spots, notes or odours that are arranged in complex patterns, melodies or blends. Receiver perception is assumed to influence preference and thus the evolution of signal design, but evolutionary biologists still struggle to understand how perception, preference and signal design are mechanistically linked. In parallel, the field of empirical aesthetics aims to understand why people like some designs more than others. The model of processing bias discussed here is rooted in empirical aesthetics, which posits that preferences are influenced by the emotional system as it monitors the dynamics of information processing and that attractive signals have effective designs that maximize information transmission, efficient designs that allow information processing at low metabolic cost, or both. We refer to the causal link between preference and the emotionally rewarding experience of effective and efficient information processing as the processing bias, and we apply it to the evolutionary model of sensory drive. A sensory drive model that incorporates processing bias hypothesizes a causal chain of relationships between the environment, perception, pleasure, preference and ultimately the evolution of signal design, both simple and complex.
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Compreensão , Emoções , Estética , HumanosRESUMO
The large body of theory on speciation with gene flow has brought to light fundamental differences in the effects of two types of mating rules on speciation: preference/trait rules, in which divergence in both (female) preferences and (male) mating traits is necessary for assortment, and matching rules, in which individuals mate with like individuals on the basis of the presence of traits or alleles that they have in common. These rules can emerge from a variety of behavioral or other mechanisms in ways that are not always obvious. We discuss the theoretical properties of both types of rules and explain why speciation is generally thought to be more likely under matching rather than preference/trait rules. We furthermore discuss whether specific assortative mating mechanisms fall under a preference/trait or matching rule, present empirical evidence for these mechanisms, and propose empirical tests that could distinguish between them. The synthesis of the theoretical literature on these assortative mating rules with empirical studies of the mechanisms by which they act can provide important insights into the occurrence of speciation with gene flow. Finally, by providing a clear framework we hope to inspire greater alignment in the ways that both theoreticians and empiricists study mating rules and how these rules affect speciation through maintaining or eroding barriers to gene flow among closely related species or populations.
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Fluxo Gênico , Especiação Genética , Preferência de Acasalamento Animal , Fenótipo , Animais , Evolução Biológica , Modelos GenéticosRESUMO
According to a recent survey, ecologists and evolutionary biologists feel that theoretical and empirical research should coexist in a tight feedback loop but believe that the two domains actually interact very little. We evaluate this perception using a citation network analysis for two data sets, representing the literature on sexual selection and speciation. Overall, 54%-60% of citations come from a paper's own category, whereas 17%-23% are citations across categories. These cross-citations tend to focus on highly cited papers, and we observe a positive correlation between the numbers of citations a study receives within and across categories. We find evidence that reviews can function as integrators between the two literatures, argue that theoretical models are analogous to specific empirical study systems, and complement our analyses by studying a cocitation network. We conclude that theoretical and empirical research are more tightly connected than generally thought but that avenues exist to further increase this integration.
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Recent studies show that epigenetic variation in the form of DNA methylation may serve as a substrate for selection. Theory suggests that heritable epigenetic marks that increase fitness should increase in frequency in a population, and these changes may result in novel morphology, behaviour, or physiology, and ultimately reproductive isolation. Therefore, epigenetic variation might provide the first substrate for selection during the course of evolutionary divergence. This hypothesis predicts that populations in the earliest stages of divergence will differentiate in their methylome prior to any genetic differentiation. While several studies have investigated natural epigenetic variation, empirical studies that test predictions about its role in speciation are surprisingly scarce. Here, we investigate DNA methylation variation using an isoschizomeric digest method, Methyl-Sensitive Amplified Polymorphism, across multiple stages of evolutionary divergence in natural populations of North American stream fishes. We show that epigenetic differentiation between methylomes is greater than genetic divergence among closely related populations across two river drainages. Additionally, we demonstrate that epigenetic divergence is a stronger predictor of the strength of behavioural reproductive isolation and suggest that changes in the methylome could influence the evolution of reproductive isolation between species. Our findings suggest a role for epigenetics not only in the initiation of divergence, but also in the maintenance of species boundaries over greater evolutionary timescales.
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Metilação de DNA , Epigênese Genética , Peixes/genética , Especiação Genética , Genética Populacional , Animais , Cruzamentos Genéticos , Feminino , Masculino , Maryland , Modelos Genéticos , Polimorfismo Genético , Isolamento Reprodutivo , RiosRESUMO
The origin of species remains a central question, and recent research focuses on the role of ecological differences in promoting speciation. Ecological differences create opportunities for divergent selection (i.e. 'ecological' speciation), a Darwinian hypothesis that hardly requires justification. In contrast, 'mutation-order' speciation proposes that, instead of adapting to different environments, populations find different ways to adapt to similar environments, implying that speciation does not require ecological differences. This distinction is critical as it provides an alternative hypothesis to the prevailing view that ecological differences drive speciation. Speciation by sexual selection lies at the centre of debates about the importance of ecological differences in promoting speciation; here, we present verbal and mathematical models of mutation-order divergence by sexual selection. We develop three general cases and provide a two-locus population genetic model for each. Results indicate that alternative secondary sexual traits can fix in populations that initially experience similar natural and sexual selection and that divergent traits and preferences can remain stable in the face of low gene flow. This stable divergence can facilitate subsequent divergence that completes or reinforces speciation. We argue that a mutation-order process could explain widespread diversity in secondary sexual traits among closely related, allopatric species.
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Meio Ambiente , Especiação Genética , Modelos Biológicos , Caracteres Sexuais , Animais , Evolução Biológica , Feminino , Genética Populacional , Masculino , Preferência de Acasalamento Animal , MutaçãoRESUMO
Theoretical and empirical research indicates that sexual selection interacts with the ecological context in which mate choice occurs, suggesting that sexual and natural selection act together during the evolution of premating reproductive isolation. However, the relative importance of natural and sexual selection to speciation remains poorly understood. Here, we applied a recent conceptual framework for examining interactions between mate choice divergence and ecological context to a review of the empirical literature on speciation by sexual selection. This framework defines two types of interactions between mate choice and ecology: internal interactions, wherein natural and sexual selection jointly influence divergence in sexual signal traits and preferences, and external interactions, wherein sexual selection alone acts on traits and preferences but ecological context shapes the transmission efficacy of sexual signals. The objectives of this synthesis were 3-fold: to summarize the traits, ecological factors, taxa, and geographic contexts involved in studies of mate choice divergence; to analyze patterns of association between these variables; and to identify the most common types of interactions between mate choice and ecological factors. Our analysis revealed that certain traits are consistently associated with certain ecological factors. Moreover, among studies that examined a divergent sexually selected trait and an ecological factor, internal interactions were more common than external interactions. Trait-preference associations may thus frequently be subject to both sexual and natural selection in cases of divergent mate choice. Our results highlight the importance of interactions between sexual selection and ecology in mate choice divergence and suggest areas for future research.
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Especiação Genética , Preferência de Acasalamento Animal , Seleção Genética , Anfíbios , Animais , Aves , Ecologia , Ecossistema , Feminino , Masculino , Mamíferos , Moluscos , Herança Multifatorial , RépteisRESUMO
A central role for sexual isolation in the formation of new species and establishment of species boundaries has been noticed since Darwin and is frequently emphasized in the modern literature on speciation. However, an objective evaluation of when and how sexual isolation plays a role in speciation has been carried out in few taxa. We discuss three approaches for assessing the importance of sexual isolation relative to other reproductive barriers, including the relative evolutionary rate of sexual trait differentiation, the relative strength of sexual isolation in sympatry, and the role of sexual isolation in the long-term persistence of diverging forms. First, we evaluate evidence as to whether sexual isolation evolves faster than other reproductive barriers during the early stages of divergence. Second, we discuss available evidence as to whether sexual isolation is as strong or stronger than other barriers between closely related sympatric species. Finally, we consider the effect of sexual isolation on long-term species persistence, relative to other reproductive barriers. We highlight challenges to our knowledge of and opportunities to improve upon our understanding of sexual isolation from different phases of the speciation process.
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Evolução Biológica , Isolamento Reprodutivo , Reprodução , Simpatria , Fenótipo , Especiação GenéticaRESUMO
Theory predicts that sexual behaviour in animals can evolve rapidly, accelerating the rate of species formation. Here we estimate the rate of speciation in Laupala, a group of forest-dwelling Hawaiian crickets that is characterized primarily through differences in male courtship song. We find that Laupala has the highest rate of speciation so far recorded in arthropods, supporting the idea that divergence in courtship or sexual behaviour drives rapid speciation in animals.
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Evolução Biológica , Gryllidae/classificação , Gryllidae/fisiologia , Comportamento Sexual Animal/fisiologia , Comunicação Animal , Animais , Feminino , Geografia , Gryllidae/anatomia & histologia , Gryllidae/genética , Havaí , Masculino , Modelos Biológicos , Filogenia , Polimorfismo Genético/genética , Seleção Genética , Caracteres Sexuais , Especificidade da Espécie , Fatores de Tempo , ÁrvoresRESUMO
In sexually dimorphic species characterized by exaggerated male ornamentation, behavioral isolation is often attributed to female preferences for conspecific male signals. Yet, in a number of sexually dimorphic species, male mate choice also results in behavioral isolation. In many of these cases, the female traits that mediate species boundaries are unclear. Females in sexually dimorphic species typically lack many of the elaborate traits that are present in males and that are often used for taxonomic classification of species. In a diverse and largely sexually dimorphic group of fishes called darters (Percidae: Etheostoma), male mate choice contributes to behavioral isolation between a number of species; however, studies addressing which female traits males prefer are lacking. In this study, we identified the dominant female pattern for two sympatric species, Etheostoma zonale and Etheostoma barrenense, using pattern energy analysis, and we used discriminate function analysis to identify which aspects of female patterning can reliably classify species. We then tested the role of female features in male mate choice for E. zonale, by measuring male preference for computer animations displaying the identified (species-specific) conspecific features. We found that the region above the lateral line is important in mediating male mate preferences, with males spending a significantly greater proportion of time with animations exhibiting conspecific female patterning in this region than with animations exhibiting heterospecific female patterning. Our results suggest that the aspects of female phenotypes that are the target of male mate choice are different from the conspicuous male phenotypes that traditionally characterize species.
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Twenty years ago, a seminal paper summarized the role of sexual selection in speciation as the coordinated evolution of (male) courtship signals and (female) preferences leading to prezygotic (behavioral) isolation between divergent lineages. Here, we discuss areas of progress that inspire an updated perspective. First, research has identified multiple mechanisms of sexual selection, in addition to female mate choice, that drive the origin and maintenance of species. Second, reviews and empirical data now conclude that sexual selection alone will rarely lead to reproductive isolation without ecological divergence, and we discuss the assumptions and possible exceptions underlying that conclusion. Finally, we consider the variable ways in which sexual selection contributes to divergence according to the spatial, temporal, social, ecological, and genomic context of speciation.
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Preferência de Acasalamento Animal , Animais , Feminino , Especiação Genética , Masculino , Isolamento Reprodutivo , Seleção GenéticaRESUMO
The snubnose darters (Percidae: subgenus Ulocentra) are a group of small, brightly colored North American freshwater fish belonging to the genus Etheostoma. Phylogenetic relationships among snubnose species have been a challenge to resolve at all levels of divergence, from the monophyly of species to deeper relationships among subgenera. Here, we used amplified fragment length polymorphisms (AFLPs) to estimate phylogenetic relationships among species from three closely related subgenera: Ulocentra, Etheostoma, and Nanostoma. With nearly complete sampling of recognized species, our analysis yielded a robust tree with statistical support at all nodes. Support was strongest for shallower relationships; support for internal nodes was either comparable to or greater than that of previous studies based on mitochondrial sequence data. Most recovered relationships were consistent with earlier hypotheses based on morphology or mtDNA sequences, with the exception of Etheostoma histrio, which was recovered as sister to Ulocentra. Our analysis indicates that careful use of AFLPs can yield statistically robust estimates of evolutionary relationships across multiple levels of divergence.
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Análise do Polimorfismo de Comprimento de Fragmentos Amplificados , Evolução Molecular , Percas/genética , Filogenia , Animais , Teorema de Bayes , DNA Mitocondrial/genética , Percas/classificação , Análise de Sequência de DNARESUMO
Reinforcement occurs when selection against hybrid offspring strengthens behavioral isolation between parental species and may be an important factor in speciation. Theoretical models and experimental evidence indicate that both female and male preferences can be strengthened upon secondary contact via reinforcement. However, the question remains whether this process is more likely to affect the preferences of one sex or the other. Males of polygynous species are often predicted to exhibit weaker preferences than females, potentially limiting the ability for reinforcement to shape male preferences. Yet, in darters (Percidae: Etheostoma), male preference for conspecific mates appears to arise before female preferences during the early stages of allopatric speciation, and research suggests that male, but not female, preferences become reinforced upon secondary contact. In the current study, we aimed to determine whether the geographically widespread darter species Etheostoma zonale exhibits a signature of reinforcement, by comparing the strength of preference for conspecific mates between populations that are sympatric and allopatric with respect to a close congener, E. barrenense. We examined the strength of preference for conspecifics for males and females separately to determine whether the preferences of one or both sexes have been strengthened by reinforcement. Our results show that both sexes of E. zonale from sympatric populations exhibit stronger conspecific preferences than E. zonale from allopatric populations, but that female preferences appear to be more strongly reinforced than male preferences. Results therefore suggest that reinforcement of female preferences may promote behavioral isolation upon secondary contact, even in a genus that is characterized by pervasive male mate choice.
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Sexual signal design is an evolutionary puzzle that has been partially solved by the hypothesis of sensory drive. Framed in signal detection theory, sensory drive posits that the attractiveness of a signal depends on its detectability, measured as contrast with the background. Yet, cognitive scientists have shown that humans prefer images that match the spatial statistics of natural scenes. The explanation is framed in information theory, whereby attractiveness is determined by the efficiency of information processing. Here, we apply this framework to animals, using Fourier analysis to compare the spatial statistics of body patterning in ten species of darters (Etheostoma spp.) with those of their respective habitats. We find a significant correlation between the spatial statistics of darter patterns and those of their habitats for males, but not for females. Our results support a sensory drive hypothesis that recognizes efficient information processing as a driving force in signal evolution.
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Percas/fisiologia , Animais , Evolução Biológica , Ecossistema , Feminino , Análise de Fourier , Masculino , Percas/genéticaRESUMO
The proposed Drosophila melanogaster L23a ribosomal protein features a conserved C-terminal amino acid signature characteristic of other L23a family members and a unique N-terminal extension [Koyama et al. (Poly(ADP-ribose) polymerase interacts with novel Drosophila ribosomal proteins, L22 and l23a, with unique histone-like amino-terminal extensions. Gene 1999; 226: 339-345)], absent from Saccharomyces cerevisiae L25 that nearly doubles the size of fly L23a. The ability of fly L23a to replace the role of yeast L25 in ribosome biogenesis was determined by creating a yeast strain carrying an L25 chromosomal gene disruption and a plasmid-encoded FLAG-tagged L23a gene. Though affected by a reduced growth rate, the strain is dependent on fly L23a-FLAG function for survival and growth, demonstrating functional compatibility between the fly and yeast proteins. Pulse-chase experiments reveal a delay in rRNA processing kinetics, most notably at a late cleavage step that converts precursor 27S rRNA into mature 25S rRNA, likely contributing to the strain's slower growth pattern. Yet, given the essential requirement for L23(a)/L25 in ribosome biogenesis, there is a remarkable tolerance for accommodating the fly L23a N-terminal extension within the structure of the yeast ribosome. A search of available databases shows that the unique N-terminal extension is shared by multiple insect lineages. An evolutionary perspective on L23a structure and function within insect lineages is discussed.
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Proteínas de Drosophila/metabolismo , Drosophila melanogaster , Proteínas Ribossômicas/metabolismo , Ribossomos/metabolismo , Sequência de Aminoácidos , Animais , Sequência Conservada , Proteínas de Drosophila/química , Proteínas de Drosophila/genética , Evolução Molecular , Proteínas de Insetos/química , Processamento Pós-Transcricional do RNA , RNA Ribossômico/metabolismo , Proteínas Recombinantes de Fusão/análise , Proteínas Ribossômicas/química , Proteínas Ribossômicas/genética , Saccharomyces cerevisiae/genética , Saccharomyces cerevisiae/crescimento & desenvolvimento , Saccharomyces cerevisiae/metabolismo , Proteínas de Saccharomyces cerevisiae/química , Proteínas de Saccharomyces cerevisiae/genética , Homologia de Sequência de AminoácidosRESUMO
Gap junction channels may be comprised of either connexin or pannexin proteins (innexins and pannexins). Membrane topologies of both families are similar, but sequence similarity is lacking. Recently, connexin-like sequences have been identified in mammalian and zebrafish genomes that have only four conserved cysteines in the extracellular domains (Cx23), a feature of the pannexins. Phylogenetic analyses of the non-canonical "C4" connexins reveal that these sequences are indeed connexins. Functional assays reveal that the Cx23 gap junctions are capable of sharing neurobiotin, and further, that Cx23 connexins form hemichannels in vitro.
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Conexinas/fisiologia , Cisteína/química , Junções Comunicantes/fisiologia , Sequência de Aminoácidos , Animais , Sequência de Bases , Conexinas/química , Primers do DNA , Junções Comunicantes/química , Células HeLa , Humanos , Hibridização In Situ , Cristalino/metabolismo , Dados de Sequência Molecular , Homologia de Sequência de Aminoácidos , Peixe-ZebraRESUMO
The higher energetic cost related to female gamete investment is classically considered the driving force behind sexual selection. This asymmetric cost of reproduction is thought to cause female preference for elaborate male ornamentation. Subsequent co-evolution of female preferences and male ornaments is thought then to lead to a greater preference for conspecific mates in females as compared to males. Thus, female choice is classically assumed to contribute more than male choice to behavioral isolation between sexually dimorphic species. However, this hypothesis fails to account for the cost of maintaining a territory, building a nest, courtship displays, ornament investment, and parental care, as seen in males of the Siamese fighting fish, Betta splendens. Here we show that male B. splendens have a greater preference for female conspecifics than females have for male conspecifics, when given a choice between conspecifics and the allopatric Betta imbellis. We hypothesize that in B. splendens, the cost of mating may be higher for males than females, and predict that male choice would contribute to behavioral isolation upon secondary contact of wild populations.
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Peixes/fisiologia , Preferência de Acasalamento Animal/fisiologia , Animais , Feminino , MasculinoRESUMO
Speciation by sexual selection is generally modeled as the coevolution of female preferences and elaborate male ornaments leading to behavioral (sexual) reproductive isolation. One prediction of these models is that female preference for conspecific males should evolve earlier than male preference for conspecific females in sexually dimorphic species with male ornaments. We tested that prediction in darters, a diverse group of freshwater fishes with sexually dimorphic ornamentation. Focusing on the earliest stages of divergence, we tested preference for conspecific mates in males and females of seven closely related species pairs. Contrary to expectation, male preference for conspecific females was significantly greater than female preference for conspecific males. Males in four of the 14 species significantly preferred conspecific females; whereas, females in no species significantly preferred conspecific males. Relationships between the strength of preference for conspecifics and genetic distance revealed no difference in slope between males and females, but a significant difference in intercept, also suggesting that male preference evolves earlier than females'. Our results are consistent with other recent studies in darters and suggest that the coevolution of female preferences and male ornaments may not best explain the earliest stages of behavioral isolation in this lineage.
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Coevolução Biológica , Especiação Genética , Preferência de Acasalamento Animal , Perciformes/genética , Animais , Feminino , MasculinoRESUMO
Identifying the manner in which reproductive barriers accumulate during lineage divergence is central to establishing general principles of species formation. One outstanding question is which isolating mechanisms form the first complete barrier to gene flow in a given lineage or under a particular set of conditions. To identify these initial reproductive barriers requires examining lineages in very early stages of divergence, before multiple reproductive barriers have evolved to completion. We quantified the strength of three postmating barriers in a pair of darter species and compared these estimates to each other and to the strength of behavioral isolation (BI) reported in a previous study. Results reveal no evidence of gametic incompatibility but intermediate levels of conspecific sperm precedence and hybrid inviability. As BI is nearly complete, our analysis comparing the strength of multiple reproductive barriers implicates the evolution of mate choice as central to both the origin and maintenance of these species. Further examination of ecological isolation and hybrid sterility is necessary to determine the role of these barriers in darter speciation.