Diversificação e hibridação em um anuro endêmico do Cerrado: genética, morfologia e comportamento
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Data
2016-10-04
Autores
Nali, Renato Christensen [UNESP]
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Universidade Estadual Paulista (Unesp)
Resumo
A configuração da paisagem e as características fenotípicas associadas ao reconhecimento de parceiros podem influenciar na estrutura genética das populações e nos processos de diversificação de uma espécie. Além disso, interações reprodutivas entre espécies distintas podem alterar a história evolutiva de linhagens com a formação de híbridos viáveis. Para investigar essas interações complexas, estudamos o anuro Bokermannohyla ibitiguara, uma espécie com reprodução prolongada, cantos elaborados, corte complexa, fêmeas seletivas e machos agressivos/territoriais. A espécie é endêmica do Cerrado e tem reprodução associada à vegetação ripária dentro e fora do Parque Nacional da Serra da Canastra (PNSC), uma zona de contato com o congênero B. sazimai. Amostramos vários riachos e desenvolvemos microssatélites para analisar a influência da topografia e cobertura vegetal na diferenciação genética. Comparamos, em seguida, morfologia e cantos através da área de distribuição e examinamos os papéis da seleção sexual, deriva genética e adaptação acústica a ambientes florestados (Hipótese da Adaptação Acústica; HAA) na diferenciação acústica. Testamos também a hipótese de que B. ibitiguara e B. sazimai podem hibridizar devido a semelhanças fenotípicas. Indivíduos de B. ibitiguara mostraram diferença genética significativa entre riachos, exceto naqueles dentro do Parque, os quais apresentaram maiores níveis de riqueza alélica e heterosigozidade. A diferenciação genética foi melhor explicada pela complexidade topográfica, bem como algumas medidas genéticas intra-populacionais. Os cantos variaram mais do que caracteres morfológicos, sugerindo uma maior pressão seletiva nesse fenótipo comportamental. Parâmetros acústicos associados com discriminação individual e/ou atração de fêmeas foram significativamente diferentes entre populações. Nem diferenciação genética nem cobertura de vegetação ripária (HAA) explicaram as diferenças acústicas entre populações, mas cantos que variaram em contraste à HAA indicaram um papel da competitividade de machos associada com aumento da densidade. Dez por cento dos indivíduos dentro do PNSC eram híbridos, apresentando valores de dissimilaridade genética sobrepostos, mas intermediários comparados às espécies parentais B. ibitiguara e B. sazimai. Características morfológicas e acústicas não foram intermediárias, mas um mosaico de fenótipos, incluindo um canto distinto em dois híbridos. Enfatizamos que a topografia pode ser um forte promotor de estruturação genética em anfíbios, e que diferenças observadas dentro e fora do Parque podem estar relacionadas à complexidade do relevo. Estratégias de conservação devem incorporar não apenas distúrbio de hábitat, como também a complexidade topográfica, principalmente em regiões ameaçadas como o Cerrado. Nossa análise fenotípica sugere que a seleção sexual promove diferenciação acústica nessa espécie por meio de reconhecimento individual, preferência de fêmeas e competitividade entre machos. Um enfoque com vários caracteres e mecanismos foi importante para explicar esses intricados processos. Além disso, são poucos os registros de híbridos em anuros com comportamento elaborado e/ou período reprodutivo prolongado, mas esse fenômeno deve ocorrer, provavelmente, devido a similaridades nos sistemas de reconhecimento e estratégias alternativas de acasalamento, como machos satélites. A diversificação multifacetada de B. ibitiguara contribui para o conhecimento nas áreas de conservação, evolução e ecologia comportamental. Acreditamos que nossos resultados podem ser aplicados a diferentes animais e biomas, devido às associações generalizadas entre indivíduos com a paisagem, com coespecíficos (do mesmo sexo ou do sexo oposto), e com outras espécies simpátricas.
Landscape configuration and phenotypic characteristics linked with mating recognition may influence population genetic structure and diversification processes. Moreover, reproductive interactions among different species may alter the evolutionary history of lineages with the formation of viable hybrids. To investigate these complex interactions we studied the treefrog Bokermannohyla ibitiguara, a species with prolonged reproduction, complex calls, elaborate courtship, choosy females and territorial/aggressive males. It is endemic to the threatened Brazilian Cerrado and breeds in streams associated with riparian forests within and outside the Serra da Canastra National Park (SCNP), a contact zone with the congener B. sazimai. We sampled many streams and developed microsatellite markers to analyze the roles of topography and land cover on genetic differentiation. We then compared morphology and calls throughout the range and examined the roles of sexual selection, genetic drift, and acoustic adaptation to forested habitats (Acoustic Adaptation Hypothesis; AAH) on call differentiation. We also tested the hypothesis that B. ibitiguara and B. sazimai may hybridize due to phenotypic similarities. Individuals of B. ibitiguara showed significant genetic differentiation among streams, except those within the Park, which had higher levels of allelic richness and heterozygosity. Genetic differentiation was best explained by topographic complexity, as were some within-population genetic measures. Calls varied more than morphology, suggesting stronger selective pressures on this behavioral phenotype. Acoustic traits associated with individual discrimination and/or female attraction showed significant population differences. Neither genetic differentiation nor riparian forest cover (the AAH) explained population acoustic differences, but call traits that varied in contrast with AAH indicated a role of male competition associated with increased density. Ten percent of individuals within the SCNP were hybrids, showing overlapping but intermediate values of genetic dissimilarities compared to parental B. ibitiguara and B. sazimai. Morphology and calls were not intermediate, but a mosaic of phenotypes, including a distinct call type in two hybrids. We underscore that topography is a strong driver of genetic structure in amphibians, and differences observed within and outside the Park may rely on the degree of topographic relief. Conservation strategies should incorporate not only habitat disturbance, but also topographic complexity, especially in threatened regions such as the Cerrado. Our phenotypic analyses suggest that sexual selection shapes call differentiation in this species in the forms of individual recognition, female preferences and intermale competition. A multi-trait and multi-mechanism approach was nevertheless crucial to explain these intricate processes. Also, records of hybridization in frogs with elaborate behavior and/or long reproductive period are underrepresented, but may also occur likely due to similarities in mating recognition systems and alternative mating tactics, such as satellite males. The multi-faceted diversification of B. ibitiguara enhances our knowledge on conservation, evolution and behavioral ecology. We believe that our results can be applied to different animals and biomes, given the widespread associations observed among individuals with the landscape, with conspecifics (within and between the sexes) and with other sympatric species.
Landscape configuration and phenotypic characteristics linked with mating recognition may influence population genetic structure and diversification processes. Moreover, reproductive interactions among different species may alter the evolutionary history of lineages with the formation of viable hybrids. To investigate these complex interactions we studied the treefrog Bokermannohyla ibitiguara, a species with prolonged reproduction, complex calls, elaborate courtship, choosy females and territorial/aggressive males. It is endemic to the threatened Brazilian Cerrado and breeds in streams associated with riparian forests within and outside the Serra da Canastra National Park (SCNP), a contact zone with the congener B. sazimai. We sampled many streams and developed microsatellite markers to analyze the roles of topography and land cover on genetic differentiation. We then compared morphology and calls throughout the range and examined the roles of sexual selection, genetic drift, and acoustic adaptation to forested habitats (Acoustic Adaptation Hypothesis; AAH) on call differentiation. We also tested the hypothesis that B. ibitiguara and B. sazimai may hybridize due to phenotypic similarities. Individuals of B. ibitiguara showed significant genetic differentiation among streams, except those within the Park, which had higher levels of allelic richness and heterozygosity. Genetic differentiation was best explained by topographic complexity, as were some within-population genetic measures. Calls varied more than morphology, suggesting stronger selective pressures on this behavioral phenotype. Acoustic traits associated with individual discrimination and/or female attraction showed significant population differences. Neither genetic differentiation nor riparian forest cover (the AAH) explained population acoustic differences, but call traits that varied in contrast with AAH indicated a role of male competition associated with increased density. Ten percent of individuals within the SCNP were hybrids, showing overlapping but intermediate values of genetic dissimilarities compared to parental B. ibitiguara and B. sazimai. Morphology and calls were not intermediate, but a mosaic of phenotypes, including a distinct call type in two hybrids. We underscore that topography is a strong driver of genetic structure in amphibians, and differences observed within and outside the Park may rely on the degree of topographic relief. Conservation strategies should incorporate not only habitat disturbance, but also topographic complexity, especially in threatened regions such as the Cerrado. Our phenotypic analyses suggest that sexual selection shapes call differentiation in this species in the forms of individual recognition, female preferences and intermale competition. A multi-trait and multi-mechanism approach was nevertheless crucial to explain these intricate processes. Also, records of hybridization in frogs with elaborate behavior and/or long reproductive period are underrepresented, but may also occur likely due to similarities in mating recognition systems and alternative mating tactics, such as satellite males. The multi-faceted diversification of B. ibitiguara enhances our knowledge on conservation, evolution and behavioral ecology. We believe that our results can be applied to different animals and biomes, given the widespread associations observed among individuals with the landscape, with conspecifics (within and between the sexes) and with other sympatric species.
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Palavras-chave
Amphibia, Bioacústica, Conservação, Genética da paisagem, Seleção sexual, Bioacoustics, Conservation, Landscape genetics, Sexual selection