ADRIÁN GARCÍA-RODRÍGUEZ
DETERMINANTES ECOLÓGICOS DE
PROCESSOS MACRO E MICRO EVOLUTIVOS
EM REGIÕES COMPLEXAS
Natal,
Rio Grande do Norte - Brasil 2018
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ADRIÁN GARCÍA-RODRÍGUEZ
DETERMINANTES ECOLÓGICOS DE
PROCESSOS MACRO E MICRO EVOLUTIVOS
EM REGIÕES COMPLEXAS
Tese apresentada à Universidade Federal do Rio Grande do Norte, como parte das exigências do Programa de Pós-Graduação em Ecologia, para obtenção do título de Doutor.
Orientador Dr. Gabriel Corrêa Costa
Co-orientador Dr. Adrian Antonio Garda
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ADRIÁN GARCÍA-RODRÍGUEZ
DETERMINANTES ECOLÓGICOS DE
PROCESSOS MACRO E MICRO EVOLUTIVOS
EM REGIÕES COMPLEXAS
Tese apresentada à Universidade Federal do Rio Grande do Norte, como parte das exigências do Programa de Pós-Graduação em Ecologia, para obtenção do título de Doutor
.
Dr. Fabricio Villalobos Membro titular externo Instituto de Ecología, A.C.
(INECOL). México
Dr. Diogo Borges Provete Membro titular externo
UFMS
Dr. Adrian Antonio Garda Membro titular interno
UFRN
Dr. Sergio Maia Queiroz Lima Membro titular interno
UFRN
__________________________ Dr. Gabriel Corrêa Costa
Orientador
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Universidade Federal do Rio Grande do Norte - UFRN Sistema de Bibliotecas - SISBI
Catalogação de Publicação na Fonte. UFRN -
Biblioteca Setorial Prof. Leopoldo Nelson -Centro de Biociências - CB
García-Rodríguez, Adrián.
Determinantes ecológicos de processos macro e microevolutivos em regiões complexas / Carlos Adrián García
Rodríguez. - Natal, 2018. 160 f.: il.
Tese (Doutorado) - Universidade Federal do Rio Grande do Norte. Centro de Biociências. Departamento de Ecologia.
Programa de Pós-Graduacão em Ecologia. Orientador: Prof. Dr. Gabriel Correa Costa.
1. Bioacústica - Tese. 2. Heterogeneidad climática - Tese. 3. Complexidade topográfica - Tese. 4. Divergência genética - Tese. 5. Especiação - Tese. 6. Macroevolução - Tese. I. Costa, Gabriel Correa. II. Universidade Federal do Rio Grande do Norte. III.
Título.
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Vive como si fueses a morir mañana. Aprende como si fueses a vivir para siempre.
Mahatma Gandhi
La ciencia se compone de errores, que a su vez, son los pasos hacia la verdad
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AGRADECIMIENTOS
Tras cuatro años de mucho aprendizaje y crecimiento personal, cierro aquí la que puedo decir -sin temor a equivocarme- ha sido la experiencia más enriquecedora de mi vida. Quedan plasmadas en estas páginas, las ideas que poco a poco fui madurando durante este tiempo, pero más que un documento que pretende hacer una pequeña contribución al conocimiento, este trabajo es el vivo reflejo de un esfuerzo (y sacrifício) conjunto, y a la vez mi humilde homenaje a todas las personas que me acompañaron en el camino.
Agradezco sobre todo a mi família, que es el centro de mi vida. A mis padres, Carlos Alberto y Carmen María, por ser mi luz, mi ejemplo y mi más grande apoyo en todo momento. Por su amor incondicional, por siempre motivarme a perseguir lo que me apasiona, por acuerpar mis decisiones y por enseñarme, desde que tengo memoria, a valorar la educación como el tesoro más preciado que me podían dar. A mis hermanas Silvi, Lauri y Marce y mis sobrinos Sofi, Ale y Amandita por su cariño, su comprensión, su complicidad, su admiración y por ser mi fuerza y motivación aún en la distancia.
A mi orientador Gabriel Costa, por ser mi principal guía en este proceso. Por su integridad profesional y su sincera amistad, por la admirable dedicación y paciencia que tiene con sus alumnos. Por su inspiradora capacidad para sacar
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lo mejor de cada uno de nosotros y estar presente y disponible aún a 7000 km de distancia. A mis co-autores y amigos Marcelo Araya, Andrew Crawford, Adrian Garda, Carlos Guarnizo, Pablo Martinez, Brunno Oliveira y Alex Pyron por toda su colaboración y críticas constructivas durante el desarrollo de estos trabajos.
A mis mentores en Costa Rica, Cachí, Fede y GB por su influencia y consejos durante mi formación como estudiante y después como profesional, por su apoyo contínuo hasta el día de hoy. A la Escuela de Biología de la Universidad de Costa Rica, especialmente a Gustavo Gutiérrez, Viviana Lang, Elsa de la O y demás funcionarios que siempre me han apoyado a lo largo de esta etapa, facilitando todos los procesos administrativos que permitieron mantener un vínculo profesional con mi querida Álma Mater.
A todos mis amigos en Costa Rica (mis “Brothers” del cole, mis queridos “Peleles” de pretil, y toda la chusma de Biolo) por siempre tener una sonrisa para recibirme y un abrazo para despedirme, por desearme lo mejor y ante todo por no dejar que la distancia nos separe. A Juanca y Eu, mis hermanitos ticos que se embarcaron conmigo en esta aventura brasilera y fueron siempre mi pedacito de Tiquicia en el exilio. A los ticos con los que en algún momento coincidí estando Brasil: Sarita, Kabeto, Boris y Hellen, gracias por la ayuda, la solidaridad y los buenos momentos. A mis grandes amigos y colegas, Pitillo,
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Erick, Victicor, Sofi Rodríguez, Sofi Granados y Bety por su ayuda en el campo y su amistad sincera.
A mis amigos en Brasil, quienes hoy son mi família lejos de casa. Mis colegas del lab Juampi, Bruninho, André, Brunnão, Tales y Felipe, por la compañia, las buenas energias y la ayuda siempre desinteresada. A mis roomies, con quiénes compartí mil historias y cuya compañia hizo todo más fácil desde el inicio, principalmente a Camura y Anita mis hermanitos y cómplices, gracias por tanto cariño y sonrisas compartidas, tamo junto sempre. A Vekinha, que le tocó aguantarme en la recta final de esta tesis, gracias por el apoyo, la paciencia y los chineos durante esta “labor de parto”. A quienes a ojos cerrados literalmente me entregaron sus casas, sus carros y sus mascotas: mis hermanos y consejeros Hélder y Carolzinha, mis amados Duka e Helo, mi otro hermano Juampi y mis queridas Tamy e Isa, gracias no sólo por todo lo que facilitaron mi vida, sino por esas grandes muestras de confianza, somos familia. A mis grandes amigos y colegas Castiele, Eliana, Vinicius y Francisco, que haciendo un esfuerzo gigantesco me visitaron en Costa Rica y también me acompañaron en mis giras de campo, recuerdos para siempre mis queridos. A mis amigas, consejeras, confidentes y hasta enfermeras Andressa y Nadia por cuidarme cuando no estuve bien y escucharme siempre que lo necesité. A Gus y Serginho
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por su sincera amistad y por siempre tener esa energía leve y una palabra adecuada para compartir.
Agradezco a todos los profesores, amigos y alumnos con quiénes coincidí en el Programa de Posgraduacao em Ecologia de la UFRN. Ha sido un placer y un honor ser parte del programa y un gusto inmenso haberlos encontrado en este camino. Todos y cada uno de ustedes forman parte de mi historia, son el más puro reflejo de la solidaridad y una muestra clara de que la amistad trasciende idiomas y fronteras... saudades galera!
Agradezco infinitamente a este Brasil querido, por recibirme de brazos abiertos, por presentarme algunos de los lugares más lindos y personas más especiales que conocí en mi vida. Por desbordarme con su diversidad cultural y sus bellezas naturales, por contagiarme de esa alegría que nunca acaba y hacerme sentir en casa. Nada de esto hubiera sido posible sin el apoyo de la Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) que financió durante 48 meses mi vida en Brasil y National Geographic Society que apoyó mi trabajo de campo en Costa Rica.
10 SUMÁRIO Agradecimientos...6 Resumo...12 Abstract...14 Introdução Geral...16
Capítulo 1. Faster amphibian speciation supports the role of mountains as biodiversity pumps Abstract……….. 26 Introdução... 27 Material e métodos... 30 Resultados... 36 Discussão... 44 Referências... 50 Material suplementar... 61
Capítulo 2. Idiosyncratic responses to drivers of genetic differentiation in the complex landscapes of Isthmian Central America Abstract………... 65
Introdução... 67
Material e métodos... 72
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Discussão... 88
Referências... 98
Material suplementar... 104
Capítulo 3. The role of geography, topography and climate in the acoustic divergence of Neotropical Diasporus frogs Abstract... 116 Introdução... 118 Material e métodos... 121 Resultados... 128 Discussão... 136 Referências... 144 Considerações finais... 158
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Resumo
As áreas de montanha do mundo cobrem menos de 15% da superfície terrestre; no entanto, elas concentram cerca de 90% dos hotspots de diversidade de espécies e 40% dos hotspots de endemismo. As evidências sugerem que fatores como a complexidade topográfica, a heterogeneidade climática e sua dinâmica histórica nas montanhas podem desempenhar um papel importante na evolução e manutenção de suas ricas biotas. Nesta tese, pretendi avaliar o papel de tais fatores tanto em escala macro (ou seja, nos padrões globais de especiação) quanto em escalas microevolutivas (ou seja, intraespecíficas de divergência genética e de traits) usando anfíbios como sistema de estudo. No primeiro capítulo, contrastei as taxas de especiação entre regiões de alta e baixa complexidade topográfica. Para este fim, usei uma filogenia quase completa de anfíbios contendo 7238 espécies (>90% da diversidade existente) para rodar uma Análise Bayesiana de Misturas Macroevolutivas (BAMM) que permite estimar as taxas de especiação. Posteriormente, projetei na geografia essa informação usando os mapas de distribuição disponíveis, para explorar padrões geográficos de especiação em anfíbios e avaliei sua associação com terrenos complexos, estimando um índice global de complexidade topográfica. Encontrei que, globalmente, as taxas de especiação são mais rápidas em regiões de alta complexidade topográfica independentemente da latitude. Desconstruí esse padrão repetindo as análises nas regiões Zoogeográficas de Wallace - levando em consideração as histórias evolutivas regionais independentes - e encontrei a mesma tendência em oito dos 11 reinos zoogeográficos. No segundo capítulo, avalio o papel relativo de diferentes componentes da paisagem na promoção da diversificação da linhagem na complexa topografia da América Central Ístmica (ACI: Costa Rica e Panamá), uma região geologicamente jovem, mas altamente biodiversa. Aqui usei DNA mitocondrial para estimar a divergência genética dentro de 11 espécies de anfíbios (9 anuros e 2 salamandras) com diferentes atributos ecológicos que ocorrem conjuntamente na região. Então, utilizei análises de Matriz Múltipla de Regressão com Randomização e Modelagem de Dissimilaridade Generalizada para quantificar o papel relativo do isolamento por distância, ambiente e resistência (topografia e adequação) na modelagem de padrões geográficos de estrutura genética dentro de cada espécie. Encontrei respostas idiossincráticas que podem refletir aspectos específicos de suas histórias de vida e poderiam dar uma visão sobre o papel da ACI como motor da especiação. No terceiro capítulo, testei se as barreiras climáticas e topográficas podem influenciar a variação dos sinais acústicos de duas espécies de sapos do gênero Diasporus. Este é um traço comportamental importante que possui características particulares que
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permitem o reconhecimento intra-específico e podem desempenhar um papel importante como mecanismo de isolamento reprodutivo. Para este capítulo, gravei vocalizações de anúncio de 170 machos de duas espécies de sapos do gênero Diasporus distribuídos na Costa Rica. Eu realizei gravações em 21 locais em todo o país, desde o nível do mar até 2800 metros de altitude. Com essa informação realizei análises bioacústicas para documentar a variação geográfica e análises correlativas de matrizes múltiplas para testar se a distância geográfica, as barreiras físicas ou climaticas entre populações, ou adaptação às condições locais podem moldar tais padrões. Para esse fim, eu incorporei análises espaciais (modelos de nicho, estimativas de rugosidade do terreno e teoria dos circuitos) para estimar níveis de isolamento das populações e ajustar um modelo de dissimilaridade generalizada para abordar esta questão. Nas duas espécies, encontrei altos níveis de variação acústica, assim como de isolamento entre populações, gerado pelos fatores testados. No entanto, somente as barreiras topográficas explicaram significativamente a variação acústica em D. diastema. Entretanto, a dissimilaridade climática e distância geográfica só possui associação marginal com os padrões de variação acústica encontrados. Em conclusão, consideramos forças que operam em uma escala local e de forma independente (por exemplo a seleção sexual, o deslocamento de caracteres ou mesmo deriva genética) poderiam então ser mais determinantes na evolução desses sinais nas espécies de estudo.
Palavras chave: Bioacústica, Complexidade Topográfica, Divergência Genética, Especiação, Genética da Paisagem, Heterogeneidade Climática, Isolamento, Macroecologia, Macroevolução, Montanhas
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Abstract
Mountain areas around the world cover less than 15% of global land surface; nevertheless, they concentrate around 90% of the hotspots of species diversity and 40% of the hotspots of endemism. Available evidence suggest that ecological factors such as landscape features (i.e topographic complexity, climatic heterogeneity and their historical dynamics) of mountains may play an important role in the evolution and maintenance of rich biotas at such regions. In my dissertation I aim to evaluate the role of such factors in both macro (i.e global speciation patterns) and microevolutionary (i.e intra-specific genetic and trait divergence) processes using amphibians as study system. In the first chapter, we tested in a global scale the Montane Pumps hypothesis, which proposes that speciation rates are faster in mountains explaining higher diversities in those regions. To this end we used a near complete Amphibian phylogeny containing 7238 species (>90% of the group’s extant diversity) and conducted a Bayesian Analysis in Macroevolutionary Admixtures (BAMM) to estimate speciation rates. Then we combined this information with available range maps to explore Amphibian geographic patterns of speciation and evaluated its association with complex terrains (mountains) by estimating a global index of topographic complexity. We found that globally, speciation rates are faster in regions of high topographic complexity independently of latitude. We repeated our analyses using the Wallace’s Zoogeographic regions, taking into account regional independent evolutionary histories, and found the same pattern in eight out of the total 11 zoogeographical realms. In a second chapter, we assess the relative role of different components of the landscape in promoting lineage diversification across the roughed topography of Isthmian Central America (Costa Rica & Panama), a geologically young but highly biodiverse region. Here we use available mitochondrial DNA to estimate genetic divergence within 10 amphibian species (8 anurans and 2 salamanders) with different biologies that co-occur in the region. Then, we use a Multiple Matrix of Regression with Randomization to assess the relative role of isolation by distance, by environment and by resistance (topography, current climate, and LGM paleoclimate) in shaping the geographic patterns of genetic structuration within each species. So far, we have not found a general force that explains genetic divergence in all studied species. Instead, we have found idiosyncratic responses that may reflect specific aspects of their life histories, such as dispersal capabilities, range size or reproductive potential. In the third chapter,
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we test how climatic and topographic barriers may influence variation in an important behavioral trait such as are advertisement calls. In anurans, such calls has species-specific features that play an important role in recognition. Then, variation in spectro-temporal features between populations has been proposed as a mechanism of reproductive isolation that may promote speciation in the long term. For this chapter I recorded advertisement calls of 170 males from 2 species of Diasporus frogs distributed in Costa Rica. I made recordings at 21 sites in all the country ranging from sea level to 2800 meters elevation. We use such information we conduct bioacoustics analyses to first document geographic variation and then test if the geographic distance, physical or ecological barriers between populations, or adaptation to local conditions could shape such patterns. To this end, we incorporate spatial analyses (niche models, terrain roughness estimations and circuit theory) to generate levels of population isolation and apply Generalized Dissimilarity Matrix test to address this question. In both species, I found high levels of acoustic variation and among population isolation derived by the tested factors. However, only topography significantly explained acoustic divergence in D. diastema while climatic dissimilarity and geographic distance are only marginally associated with the patters of acoustic variation in D. hylaeformis. In conclusion, other forces operating independently in the local scale -such as sexual selection, character displacement or genetic drift- may be more determinant in the evolution of acoustic signals in these species.
Keywords: Bioacoustics, Climatic Heterogeneity, Genetic Divergence, Isolation, Landscape Genetics, Macroecology, Macroevolution, Mountains, Speciation, Topographic Complexity
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INTRODUÇÃO GERAL
Um dos fenômenos naturais mais amplamente documentados é a distribuição desigual que tem a diversidade em múltiplas dimensões (Menge and Sutherland 1976). Os padrões de riqueza de espécies, variam através do espaço, do tempo e dos clados: algumas regiões são mais diversas que outras (Hillebrand 2004), a composição da diversidade hoje não é a mesma que no passado (Johnson 2009) ainda, alguns grupos taxonômicos são muito diversos, outros contem poucos representantes (Wiens 2011). Entender o porquê dessa variação tem se tornado um dos maiores objetivos de pesquisa na intersecção da ecologia e evolução, gerando hipóteses derivadas dessas duas áreas da ciência.
Na escala espacial, uma das mais extremas variações na distribuição da diversidade acontece em áreas de topografias irregulares. Globalmente os sistemas montanhosos tem uma distribuição desigual que abrange somente uma oitava parte da superfície da terra (Antonelli 2015, Körner et al. 2017). No entanto, essas regiões concentram altas riquezas de espécies, sendo que 90% dos hotspots de diversidade e 40% dos hotspots de endemismo ocorrem em áreas de montanha (Myers et al. 2000, Orme et al. 2005). A tendência que tem as regiões de alta complexidade topográfica para suportar altos números de espécies é um padrão bem documentado em diversos grupos animais e vegetais (Ruggiero and Hawkins 2008). Porém, os determinantes ecológicos e os
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mecanismos macro e micro evolutivos que geram essa diversidade biótica ainda são pouco conhecidos.
Tem-se sugerido que as regiões montanhosas poderiam agir como motores de especiação, pelo efeito duplo que as topografias complexas e os fortes gradientes ambientais contidos nelas podem ter nos processos de divergência genética (Funk et al. 2016). As configurações irregulares de topos de montanha e vales alternados representam mosaicos de habitats favoráveis e desfavoráveis (Kozak and Wiens 2006), que aumentam o isolamento entre populações e em consequência a probabilidade de especiação alopátrica (Orr and Smith 1998, Moritz et al. 2000, Rull 2005, Guarnizo et al. 2009). Complementariamente, os amplos espectros ambientais representados em curtas distâncias ao longo dos gradientes altitudinais (Graham et al. 2014, Merckx et al. 2015), oferecem condições ideais em que a especiação ecológica em parapatria pode ocorrer (Rundle and Nosil 2005). Nessas circunstâncias, as pressões locais poder promover divergência entre populações, levando ao surgimento de novas espécies, mesmo na ausência de barreiras físicas maiores (Knox and Palmer 1995, Graham et al. 2004, Caro et al. 2013, Chapman et al. 2013).
Dentro de uma perspectiva macro ecológica, a montagem de comunidades e riqueza de espécies numa região especifica, num dado momento,
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é determinada pelos processos de especiação, extinção e dispersão (Hutter et al. 2013). Portanto, a identificação dos fatores que potencialmente influenciam nestes processos é crucial para entender a origem dos amplos padrões de diversidade atual. Em escalas mais locais, as abordagens desenvolvidas nas áreas da filogeografia e genética da paisagem tem sido úteis para abordar essa questão com maior resolução espacial mas menor alcance taxonômico e geográfico.
Nesta tese avalio em diferentes escalas geográficas de que forma as paisagens complexas determinadas por regiões montanhosas possuindo perfis climáticos heterogêneos influenciam em processos evolutivos que contribuem para a formação dos padrões biológicos que observamos. O meu interesse foi primeiramente abordar essa questão tentando obter o ‘big picture’ da generalidade de certos padrões macro evolutivos em escala global; ao mesmo tempo, que procurei aprofundar numa maior resolução, testando o rol que tem certos atributos físicos e ecológicos da paisagem na geração de pressões locais que influenciam os processos micro evolutivos de diferenciação genética e divergência acústica no espaço. Para atingir esses objetivos eu incorporei diversas análises evolutivas, conceitos de genética de populações, abordagens da ecologia do comportamento e ferramentas de machine learning para projetar
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no espaço múltiplos padrões de variação e avaliar quais são as forças que lós explicam melhor.
No primeiro capítulo, testei em escala global se existe uma relação entre taxas de especiação mais rápidas e regiões topograficamente complexas, que potencialmente poderia explicar maiores diversidades nessas regiões. Para este fim, usei uma filogenia quase completa de anfíbios para estimar dinâmicas evolutivas. Posteriormente, espacializei essa informação para explorar padrões geográficos de especiação em anfíbios e avaliei sua associação com terrenos complexos, estimando um índice global de complexidade topográfica. No segundo capítulo, avalio o papel relativo de diferentes componentes da paisagem na promoção da diversificação da linhagem na complexa topografia da América Central Ístmica (ACI: Costa Rica e Panamá). Aqui usei DNA mitocondrial para estimar a divergência genética dentro de 11 espécies de anfíbios que ocorrem conjuntamente na região. Posteriormente quantifiquei o papel relativo do isolamento por distância, ambiente e resistência (topografia e adequação bioclimatica) na modelagem de padrões geográficos de estrutura genética dentro de cada espécie. No terceiro capítulo, testei como as barreiras climáticas e topográficas podem influenciar a variação nas chamadas de anuncio de duas espécies de sapos do gênero Diasporus. Para este capítulo, gravei vocalizações de anúncio de 170 machos em 21 locais na Costa Rica,
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desde o nível do mar até 2800 metros de altitude. Com essa informação eu documentei a variação acústica intraespecifica e testei se a distância geográfica, o isolamento gerado pela topografia e o clima, ou a adaptação às condições locais podem moldar tais padrões.
Referências
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Caro, L. M. et al. 2013. Ecological speciation along an elevational gradient in a tropical passerine bird? - J. Evol. Biol. 26: 357–374.
Chapman, M. A. et al. 2013. Genomic divergence during speciation driven by adaptation to altitude. - Mol. Biol. Evol. 30: 2553–2567.
Funk, W. C. et al. 2016. Elevational speciation in action? Restricted gene flow associated with adaptive divergence across an altitudinal gradient. - J. Evol. Biol. 29: 241–252.
Graham, C. H. et al. 2004. Integrating phylogenetics and environmental niche models to explore speciation mechanisms in dendrobatid frogs. -
Evolution. 58: 1781–93.
Graham, C. H. et al. 2014. The origin and maintenance of montane diversity: integrating evolutionary and ecological processes. - Ecography. 37: 711– 719.
Guarnizo, C. E. et al. 2009. The relative roles of vicariance versus elevational gradients in the genetic differentiation of the high Andean tree frog, Dendropsophus labialis. - Mol. Phylogenet. Evol. 50: 84–92.
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Hillebrand, H. 2004. On the generality of the latitudinal diversity gradient. - Am. Nat. 163: 192–211.
Johnson, C. N. 2009. Ecological consequences of Late Quaternary extinctions of megafauna. - Proc. R. Soc. B 276: 2509–2519.
Knox, E. B. and Palmer, J. D. 1995. Chloroplast DNA variation and the recent radiation of the giant senecios (Asteraceae) on the tall mountains of
eastern Africa. - Proc. Natl. Acad. Sci. U. S. A. 92: 10349–10353.
Körner, C. et al. 2017. A global inventory of mountains for bio-geographical applications. - Alp. Bot. 127: 1–15.
Kozak, K. H. and Wiens, J. J. 2006. Does niche conservatism promote
speciation? A case study in North American salamanders. - Evolution. 60: 2604–21.
Mayr, E. 1963. Animal species and evolution. - Eugen. Rev. 55: 226–228. Menge, B. A. and Sutherland, J. P. 1976. Species Diversity Gradients:
Synthesis of the Roles of Predation, Competition, and Temporal Heterogeneity. - Am. Nat. 110: 351.
Merckx, V. S. F. T. et al. 2015. Evolution of endemism on a young tropical mountain. - Nature 524: 347–350.
Moritz, C. et al. 2000. Diversification of rainforest faunas: an integrated molecular approach. - Annu. Rev. Ecol. Syst. 31: 533–563.
Myers, N. et al. 2000. Biodiversity hotspots for conservation priorities. - Nature 403: 853–8.
Orme, C. D. L. et al. 2005. Global hotspots of species richness are not congruent with endemism or threat. - Nature 436: 1016–1019.
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Orr, M. R. and Smith, T. B. 1998. Ecology and speciation. - Trends Ecol. Evol. 13: 502–506.
Ruggiero, A. and Hawkins, B. A. 2008. Why do mountains support so many species of birds? - Ecography (Cop.). 31: 306–315.
Rull, V. 2005. Biotic diversification in the Guayana Highlands: a proposal. - J. Biogeogr. 32: 921–927.
Rundle, H. D. and Nosil, P. 2005. Ecological speciation. - Ecol. Lett. 8: 336– 352.
Wiens, J. J. 2011. The causes of species richness patterns across space, time, and clades and the role of “ecological limits”. - Q. Rev. Biol. 86: 75–96. Wiens, J. J. and Graham, C. H. 2005. Niche Conservatism: integrating
evolution, ecology, and conservation biology. - Annu. Rev. Ecol. Evol. Syst. 36: 519–539.
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CAPÍTULO I*
Faster amphibian speciation supports the role of mountains
as biodiversity pumps
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Faster amphibian speciation supports the role of mountains as biodiversity pumps
Adrián García-Rodríguez1,2, Pablo A. Martínez3, Brunno F. Oliveira1,4, R. Alexander Pyron5 & Gabriel C. Costa6
1 Departamento de Ecologia, Universidade Federal do Rio Grande do Norte, Natal - RN, Brasil, 59078-900
2 Escuela de Biología, Universidad de Costa Rica, San Pedro, 11501-2060 San José, Costa Rica.
3 PIBi Lab. (Laboratorio de Pesquisas Integrativas em Biodiversidade), Programa de Pós-Graduação em Ecologia e Conservação, Universidade Federal do Sergipe, São Cristóvão, Brasil
4 Department of Wildlife Ecology and Conservation, University of Florida, Gainesville, FL 32611-0430, USA
5 Department of Biological Sciences, The George Washington University, 2023 G Street NW, Washington, DC 20052, USA
6 Department of Biology, Auburn University at Montgomery, Montgomery, AL 36124, United States of America.
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ABSTRACT
Continental mountain areas cover less than 15% of global land surface; nevertheless, around 90% of the hotspots of species diversity and 40% of the hotspots of endemism are concentrated in these regions. Such high diversities could be explained by higher diversification rates in regions of high topographic complexity, giving mountains the character of speciation pumps. We specifically focused on testing whether speciation is faster in mountains by conducting macro evolutionary analyses on a near complete Amphibian phylogeny and evaluating geographic patterns of this evolutionary rate. We accounted for the role of topographic complexity on speciation patterns across the globe and within zoogeographic realms. We found that globally, speciation rates are higher in mountainous areas. At a regional scale, we found the same pattern for most zoogeographical realms. Moreover, clades showing the fastest speciation rates are groups with predominantly montane distributions. Our study bolsters the importance of mountains as engines of speciation at different geographical scales. Due to their remoteness, the real contribution of such areas to the origin and maintenance of global biodiversity is probably still underestimated. These facts and the risk these regions face from global change suggests that mountains around the globe should be conservation priorities in local and regional agendas.
Keywords: Amphibians, BAMM, Macroecology, Macroevolution, Topographic Complexity
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BACKGROUND
Nearly one-third of the world’s terrestrial species diversity is concentrated in regions of high topographic complexity [1]. High diversity in mountain regions is a well-documented pattern [2–4], reported for numerous taxa and regions [5]. In Central and North America for example, mammal diversity is greater in regions dominated by mountains and complex reliefs [6]. Likewise, peaks of species richness and endemism of Afrotropical avifauna occurs within mountains and mountain-lowland complexes [7] . Worldwide, most global centres of vascular plant richness (>5000 species per 10,000 km2) are located in regions dominated by mountainous areas such as Costa Rica-Chocó, Tropical Eastern Andes, Atlantic Brazil, Northern Borneo and New Guinea [8]. As a consequence, despite continental mountain areas covering less than 15% of global land surface [9], around 90% of the hotspots of species diversity and 40% of the hotspots of endemism [10,11] are concentrated in these regions.
Although this pattern has been reported for several taxa and across different regions [5], we still lack a comprehensive understanding of the mechanisms that drive higher diversity in mountains [12]. From an evolutionary perspective, montane systems have been hypothesized to be engines of diversification, because of their potential to drive speciation, both in allopatry and parapatry [13]. Evidence of allopatric speciation [14] promoted by the vicariant settings implicit in complex topographies have been widely documented in a variety of taxa [15–17]. For many
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groups, the irregular configuration of alternate mountaintops and valleys represent mosaics of favourable and unfavourable habitats [18] that increases isolation among populations, thereby increasing opportunities for allopatric speciation [19]. Moreover, the distribution of such suitable regions has varied in response to historical climatic oscillations, increasing allopatric diversification in the mountains [20]. Other features of mountains are the wide environmental spectrums they cover in short distances along their elevational gradients [12,21]. These transitions offer ideal conditions where ecological speciation in parapatry can take place [22]. In these circumstances, local pressures can drive adaptive divergence between populations, leading to the formation of new species, in the absence of hard geographic barriers [23–26].
Whether by allopatric or parapatric speciation, the idea that mountains act as cradles of biodiversity has been supported in several studies that linked the chronology of orogenic events to radiations of clades. For instance, the rise of the Tibetan Plateau seems to have triggered the rapid radiation of glyptosternoid catfishes [27]; ranid frogs [28] and plants of the families Asteraceae and Fabaceae [29,30]. Similarly, accumulating evidences suggests that the Andes uplift impacted evolutionary dynamics of Neotropical taxa such as hummingbirds from the genus Adelomyia [31], butterflies from the subtribe Oleriina [32], and a variety of angiosperm clades [33–36].
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Since the processes of speciation, extinction and dispersal are the ultimate determinants of diversity occurring in a given geographic region [37], identifying potential factors that drives these processes is crucial to understand the origin and distribution of past, present, and future biodiversity. Recently, several hypotheses based on this evolutionary framework have been proposed to explain the rich biotas in montane regions [12]. One of them is the Montane species pump hypothesis, which predicts that clades occurring at mountains have higher rates of net diversification [38] likely as consequence of their higher rates of speciation. Evidence supporting this model has been reported for Mesoamerican hylid frogs as well as for tanagers and butterflies from the Andes; in these cases, montane clades showed higher speciation rates than those whose ranges are restricted to lowlands [38–40].
However, the few studies testing whether complex topographic regions are speciation pumps were too restrictive in terms of their phylogenetic scope (i.e. few specific clades were analysed) and geographical extent (i.e. explored only local to regional scales), which limits our ability to determine the generality of topographic complex regions as speciation pumps. Here, we assess the prediction that complex topographies promote faster speciation rates. To do this, we use amphibians as a study system, and integrate global information on species distributions, terrain complexity and novel analyses on evolutionary dynamics across a nearly complete
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phylogeny of the group. Amphibians are a particularly suitable study system to test this hypothesis because they represent an ancient radiation (~7700 species,
www.amphibiaweb.org), with widespread latitudinal and altitudinal distribution across the globe [41] and a growing availability of phylogenetic information [42,43]. In addition, their high philopatry [44], restricted dispersal capabilities [45], limited osmotic tolerance [46], high sensitivity to temperature in early developmental stages [47], and adaptations to particular elevations [48,49] bond their evolutionary fate strongly to their geographic settings, providing a valuable opportunity to investigate the forces shaping speciation patterns in montane regions.
METHODS
Amphibian Phylogeny
When inferring diversification dynamics through time, inclusion of all lineages in focal clades or regions has been proven to be of special importance [50,51]. Considering the known sampling bias towards particular clades and specific geographic areas as well as the global character of our approach, we attempted to improve the performance of our analysis by using a tree containing as many species as possible, even those lacking molecular data. Recent practice enables the incorporation of lineages lacking genetic data on tree inference using a given set of priors on branching times [52]. Then, we based our macroevolutionary analyses on
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recently published trees which to date represent the most complete amphibian phylogenetic inference [53]. These trees were constructed using the Phylogenetic Assembly with Soft Taxonomic Inferences (PASTIS) approach [52] updating an existing molecular supermatrix [43] that contains sequence data (5 mitochondrial and 10 nuclear genes) for ~56% of extant amphibian species. A Maximum-Likelihood (ML) topology for these species then served as backbone for a set of 10, 000 trees containing 7,238 species, which represent ~94% of the known extant amphibian diversity and includes most families, subfamilies and genera. For detailed description on dating and tree construction, see [53].
Amphibian Evolutionary Dynamics
In order to estimate evolutionary rates, we modelled macroevolutionary dynamics across the amphibian phylogeny using Bayesian Analysis of Macroevolutionary Mixtures (BAMM) [54]. BAMM models complex dynamics of speciation, extinction and trait evolution on phylogenetic trees, by detecting and quantifying heterogeneity on those rates while exploring a vast parameter-space of diversification models via reversible Markov Chain Monte Carlo (MCMC) [55]. This approach is useful since it does not assume that rates of speciation and extinction are constant, and can account for rate variation through time and among lineages [56]. The performance and theoretical foundations of BAMM has recently
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received criticism, mainly dealing with the algorithm’s likelihood function, the posterior distribution on the number of rate shifts and the reliability of its diversification rate estimates [57]. However, BAMM’s authors have provided detailed evidence to clarify those concerns and demonstrated satisfactory and consistent performance of the method [58]. BAMM analysis provide speciation and extinction rates per species as direct output, and is possible to estimate net diversification rates by subtracting extinction rates from speciation rates [59]. However, we decided to focused our analyses on speciation rates, because they can be estimated with much more confidence than extinction rates, for which confidence intervals tend to be large, even when all assumptions of the inference model are satisfied [60]. Details of this analysis are provided in the supplementary material (electronic supplementary material, text S1).
Spatial patterns of Amphibian speciation
We used geographical range maps for 6311 amphibian species obtained from the IUCN (www.iucnredlist.org). These maps represent approximately 85% of the known extant amphibian species (~7500 species, www.amphibiaweb.org). Although we estimated macro evolutionary dynamics using ~94% of amphibian diversity represented in our phylogenetic tree, available range maps limited our analyses to a smaller number of species projected in the geographical space. We overlaid species
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range maps in a 1x1 degree global grid and extracted species presence-absence within each grid cell, creating a presence-absence matrix for the 6311 species in the phylogeny that had range maps available. These analyses were conducted in the R package LetsR [61]. We further estimated speciation rates based on species composition within each grid cell.
Some authors have argued that species ranges may be too dynamic and this would mask any potential relationship between current distributions and the geography of speciation [62]. However, strong evidence supporting range stasis is available in the literature for a variety of organisms, from fossil molluscs to living insects and mammals [63–65]. We considered that it is unlikely that all species have altered their ranges enough to remove geographical signal from their past distribution. Most amphibian species have low dispersal ability [66] and are highly sensitivity to environmental conditions, resulting in a high proportion of species of small range sizes [67,68]. Therefore, the effects of range dynamics on the geographical signal we are investigating should be a minor concern in this study, especially at the scales we are working.
Topographic complexity
In order to have an informative proxy of geomorphologic heterogeneity, we generated a global index of topographic complexity (TC). Using a global layer of
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elevation at 30-second resolution (~1km at the equator, http://www.worldclim.org/) we calculated the standard deviation of differences between 100x100 adjacent elevations. This procedure has been demonstrated to more accurately represent topographic roughness than elevation range, which only indicates the strength of a gradient within a cell [69]. We projected our TC layer to match the 1x1 degree resolution of our species distribution dataset.
Amphibian speciation in topographic complex regions
TC is not evenly distributed around the world [70]. This pattern reflects in our metric of TC, for which the number of cells with low values widely exceeds the number of cells with high values across the globe (Fig. 1c). To account for this, we created two categories: low topographic complexity (LTC) and high topographic complexity (HTC). We considered as HTC cells that have a complexity index value higher than 300. Our complexity index is correlated with altitude and a value of 300 assures that we are selecting regions that are at least 600 meters elevation. This approach is conservative considering that Körner et al. (2017) defined montains as those areas above 200m elevation.
To test the montane pump hypothesis, we compared speciation rates between LTC and HTC regions. According to this hypothesis, HTC areas should show higher speciation rates than LTC areas. HTC cells represent only a small fraction of the
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total number of cells across the globe (2196 cells or 14.5% of all cells analysed). Therefore, to test for significant differences between LTC and HTC speciation rates we used a rarefaction procedure [71]. We calculated the average speciation rate for all HTC cells and next, randomly sampled 2196 cells from the LTC and calculate the average speciation rate. Finally, we repeated this procedure 10,000 times, generating a distribution of average speciation rates for LTC. The observed average for HTC was then compared with the LTC generated distribution to assess significance. In order to test how speciation rates vary between LTC and HTC regions at different latitudes, we conducted this same analysis within the updated zoogeographic realms, a classification that defines robust biogeographic units based on global distributions and phylogenetic relations from over 20,000 world´s vertebrate species [71]. Therefore, using this delimitation also allows us to consider the evolutionary histories of the different zoological Realms.
Finally, we provided some examples to illustrate general patterns, where we compared mean speciation trajectories between predominantly montane groups and groups mainly distributed in adjacent lowlands. For this, we gathered species-specific information on elevation ranges for species belonging to several montane or lowland genera available at http://www.iucnredlist.org. We used this information to plot elevational distribution pattern for each genus and extract their respective
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speciation rates to visualize how they vary through time and how different they are between lowland and montane clades.
RESULTS
Evolutionary Dynamics
When checking for convergence of BAMM runs, we obtained values of 210.66 and 418.99 for the effective sample sizes of the log-likelihood and the number of shift events present in each sample respectively. These values have been shown to be reasonable for very large datasets confirming convergence of our analyses [72]. We found strong evidence for heterogeneous diversification dynamics in amphibians. Based on the values of posterior quasi-probability across all bootstrap replicates from post burn-in BAMM, we found support for 45 evolutionary rate shifts (mean = 48.35; median = 48) (electronic supplementary material, Fig S1). We focus our discussion on speciation rates dynamics, however since we found a high positive linear correlation between speciation and net diversification rates (Pearson's r = 0.97, p < 0.001) we consider that speciation might provide good insights on the diversification of amphibians.
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Figure 1. Species richness based on the distribution of 6311 species (A); mean speciation rate (B) and topographic complexity (C) per 1° grid cell in a global scale.
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Geographic patterns of Amphibian speciation
Mean amphibian speciation-rates are unevenly distributed across the world. Speciation rates show an inverse latitudinal gradient in the New World, with faster speciation rates towards the poles. In the Old World speciation rates increase only towards northern latitudes, while regions such as Africa, Madagascar and Western Australia are characterized by low speciation rates. A major portion of Southeast Asia and the Neotropical Region show low to intermediate mean speciation rates (Fig. 1).
We detected that speciation rates vary widely within regions. Such variability peaks in Mesoamerica, Patagonia and North America (Fig. 2), where there is a mixture of groups with both fast and slow speciation rates (Fig. 2). Rapidly diversifying groups are concentrated in the Neotropical, Panamanian, Nearctic and Australian regions. In contrast, we found, lowest values of speciation rates in western Africa and most of the Palearctic region (Fig. 2).
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Topographic complexity as driver of speciation
At the global scale, we found faster speciation rates in HTC regions than in LTC regions (HTCmean=0.0679, LTCmean=0.0651, p-value <0.0001). Considering independent evolutionary histories, we applied the same approach across global biogeographic realms. At this regional scale, we found the same pattern of faster speciation in HTC in eight out 11 realms (Fig. 3, Table 1). In addition, speciation rates also tended to be higher in HTC in the realms were statistical difference were not significant (i.e., Afrotropical, Madagascan and Nearctic realms) (Table 1, Fig 3).
Table 1. Differences in mean speciation rates between LTC and HTC areas in global scale and within the 11 Zoogeographical regions of the world.
Region Mean Speciation Rate in HTC Mean Speciation Rate in LTC SD of Speciation Rates in LTC P-value Global 0.0679 0.0651 0.0004 <0.001 Neotropical 0.0605 0.0551 0.0002 <0.001 Afrotropical 0.0532 0.0523 0.0005 0.969 Madagascan 0.0500 0.0483 0.0008 <0.001 Australian 0.0648 0.0546 0.0005 <0.001 Nearctic 0.0724 0.0717 0.0002 0.996 Oceania 0.0605 0.0560 0.0002 <0.001 Oriental 0.0639 0.0592 0.0002 <0.001 Panamanian 0.0642 0.0604 0.0004 <0.001 Saharo-Arabian 0.0685 0.0639 0.0006 <0.001 Sinojapanese 0.0746 0.0713 0.0004 <0.001 Palearctic 0.0682 0.0651 0.0002 <0.001
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Figure 3. Mean speciation rates for LTC and HTC areas in a global scale and within the different zoogeographic realms. Histograms represent the distribution of values obtained after resampling 10 000 times the number of cells in HTC from the pool of LTC cells. Dashed lines represent the mean values of speciation rate for LTC (blue) and HTC (red) regions.
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Faster speciation rates are generally associated with clades that predominantly inhabit HTC areas. In the New World for example, those clades occur in several Andean, Mesoamerican and North American mountain chains, and in a series of islands dominated by steeped topographies such as Jamaica and Dominican Republic. In the Old World, speciation rates peak at the Himalayans and other major mountainous systems in China, Philippines and Papua New Guinea. In Australia, we found speciation rates maxima similar to those of the other regions although they were not exclusively associated to mountainous areas.
When comparing speciation rates across the phylogeny, we found faster rates in salamanders (Caudata = 0.0781±0.034; Anura = 0.053±0.016; Gymnophiona=0.028±0.001; p = 0.0054, Df = 2). Differences are also significant among Amphibian families (p<0.0001, Df = 75) as well as among families within the orders Anura (p<0.0001, Df = 57) and Caudata (p<0.0001, Df = 8). Mean speciation rates among Gymnophiona families did not differ significantly (p = 0.077, Df = 8). At the genus level, the fastest speciation rates occur in the Patagonian spiny frogs Alsodes (mean = 0.1934±0.006, n = 18). Other anuran genera showing high rates of speciation are the bufonid genera Rhinella and Atelopus, ranids of the genera Rana, Odorrana, Babina and Amolops, as well as the New World direct developing frogs of the genus Brachycephalus. Salamanders of the family Plethodonthidae, which includes genera such as Bolitoglossa, Eurycea, Pseudoeurycea,
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Batrachoseps, Thorius, Nototriton and Oedipina (electronic supplementary material, Fig S2) showed the highest speciation rates at the family level (mean = 0.0982±0.0383, n = 450).
Figure 4. Comparative patterns of altitudinal distributions and speciation
trajectories for contrasting montane and lowland anuran genera. A-B. The bufonid highland genus Atelopus from Northern Andes, a closely related genus (Rhaebo)
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and a highly diverse hylid genus (Scinax), both distributed in lower elevations mainly the adjacent Amazon Basin; C-D. Three centrolenid genera from the Andean and Mesoamerican Region presenting different altitudinal distributions: Hyalinobatrachium with the lower elevation range and most species occurring below 1000 m.a.s.l and Nymphargus and Centrolene with mean altitudes around 2000 m.a.s.l; E-F. Three Ranid genera from the Old World with different patterns of altitudinal distribution: Pelophylax and Meristogenys with most of their
representatives occurring below 500 m.a.sl and Odorrana with a peak of diversity above 1000 m.a.s.l and several species reaching 3000 m.a.s.l
As predicted, most of the rapidly diversifying clades showed predominantly montane distributions. To exemplify this trend, we compared speciation through time plots between some of these montane genera and lowland genera. To make it comparable, we contrast genera with similar richness. In all cases, speciation rates were higher in clades that are mostly montane, and the differences were constant through the evolutionary history of these groups, depicting historical differences in their speciation trajectories (Fig 4).
DISCUSSION
We found that speciation rates are generally higher in HTC regions than in LTC regions at a global scale, in concordance with the montane-pump hypothesis. In addition, our results provide evidence showing that maximum speciation rates are generally associated with clades that predominantly inhabit HTC regions. These includes several Andean ranges, Mesoamerican mountain chains, various Sierras in
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North America, and a series of islands dominated by steeped topographies such as Jamaica and Hispaniola in the Western Hemisphere. In the Old World, the Himalayans and other major mountainous systems in China, Philippines and Papua New Guinea exhibit similar dynamics. This suggests that highly complex reliefs around the globe, independently of their latitude, have an important role as engines of speciation. It also suggests that these dynamics are specific to the geographical setting of montane regions generally, and not specific geographic areas or traits possessed by specific lineages that confer increased diversification.
A growing body of literature provide evidence supporting the role of mountains as species cradles for numerous taxa. A few examples are the Australasian Sky Islands [73,74], the Hendguan Mountains [75,76], and the Anatolian Mountains in the eastern hemisphere [75,76]. In the New World, evidence of such tendency has been documented in regions such as the Andes [32,75–80] and the North American Sky Islands [81,82]. Such studies have often focused on few clades and specific geographic regions that exhibit high diversity. Our study is the first to our knowledge to contrast speciation rates between HTC and LTC regions at global scale. We provide evidence of the general importance of mountain ranges as speciation pumps. Importantly, our results suggest that mountains affect speciation rates independently of region, diversity, or specific lineage in amphibians.
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Across the phylogeny, we found that salamanders have the highest mean speciation rates among Amphibians, followed by anurans and caecilians. Salamanders are abundant in North temperate regions where seven of the 10 families in the order are distributed (www.amphibiaweb.org). Within the order, we found the highest speciation rates in Plethodontidae, a family whose representatives reach the tropics of the western hemisphere [83]. The major radiation of this family is the Neotropical tribe Bolitoglossini, which occurs throughout complex topographies within Mesoamerica, and contains nearly 300 species, that accounts for over 65% of the species in the family and 43% of the diversity in the order [84].
Among anurans, speciation rates also peak in montane-associate clades. Fastest speciation rates occur in the genera Alsodes [85] and Eupsophus from the Patagonian Andes (despite the low diversity of this region) and bufonids such as the Harlequin toads of the genus Atelopus which have mainly radiated in the highlands of the northern Andes [17]. In mountain ranges of south eastern and eastern Asia, ranids of the genus Odorrana [86–88] also rank among the anuran clades with the highest means of speciation rate. As examples of these evolutionary contrasts, we compared altitudinal distributions and speciation trajectories within these genera with those of closely relatives or similarly diverse clades occurring in adjacent lowlands. In all cases, it is evident that montane clades have higher speciation rates and these differences have been constant through time (Fig 4).
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Rates of speciation can be influenced by both intrinsic biological attributes and extrinsic environmental factors [13,89]. Some of the latter factors may be magnified in topographically complex landscapes. For example, characteristic rugged reliefs in mountainous regions are more likely to impose physical barriers, fragmenting species ranges and promoting geographical isolation [14,16,17,21,90]. Furthermore, altitudinal gradients in these complex landscapes, provide heterogeneous environmental conditions that could promote ecological specialization and niche divergence based on trait differences [91,92]. Both scenarios restrict gene flow, augmenting founder effects and driving speciation whether in allopatric or parapatric conditions [43,85]. For groups with low dispersal rates such as amphibians, these conditions appear to have a major impact on the processes of incipient population differentiation, and ultimately, speciation [43,92].
Our results also provide insights on the latitudinal and zoogeographic patterns of amphibian speciation. We found high latitudinal variance in amphibian speciation rates. Such variability is strikingly decoupled from the well-documented latitudinal diversity gradient (LDG) present in amphibians and many other groups [94] . For example, mean speciation rates for all amphibians are higher in temperate zones of both the New and the Old world, while lower mean rates were concentrated in more speciose regions such as Africa, Madagascar, and Western Australia. Other hotspots of diversity, including a major portion of Southeast Asia and the Amazon Basin [60],
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showed intermediate mean speciation rates. We suggest that the great variability of speciation rates in speciose areas with heterogeneous species compositions may obscure the latitudinal patterns of speciation. However, future studies should explore the relation between latitude and speciation rates more deeply, in order to understand the main evolutionary forces shaping the LDG in amphibians.
CONCLUSIONS
Our findings bolster the general importance of mountains as engines of speciation at different geographical scales and independently of latitude. However, due to their remote conditions, many mountain ranges remain unexplored and their real contribution to the origin and maintenance of global biodiversity is still underestimated. For these reasons and the risk these regions face during ongoing global changes [71], mountains around the world must be considered conservation priorities in local and regional agendas. The evidence presented here highlights the role of such areas in the evolutionary history of modern patterns of diversity; further efforts must be oriented to increase the knowledge of these areas to inform future decisions for the conservation of their particular biotas.
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DATA ACCESSIBILITY
The phylogeny used here is a random tree extracted from the topologies made available by Jetz & Pyron [53] at https://vertlife.org/files_20170703/#amphibians. TCI was calculated using an elevation layer available at www.worldclim.org at 30 secs resolution. R code and associated files are available as electronic supplementary material
AUTHORS' CONTRIBUTIONS
AGR conceived of the study, discussed design, conducted analyses and drafted the manuscript. PAM conceived of the study and participated in data analyses. BFO participated in data analyses. RAP participated in data analyses. GCC conceived of the study, discussed design of analyses and drafted the manuscript. All authors improved the draft of the manuscript and gave final approval for publication.
COMPETING INTERESTS We have no competing interests.
FUNDING
AGR was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior, Brazil. GCC thanks CNPq produtivity grant 302297/2015-4. RAP was
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supported by US NSF grant DEB-1441719 and DEB-1655737. BFO thanks
University of Florida for providing generous support.
ACKNOWLEDGEMENTS
We thank Marcelo Araya and Juan Pablo Zurano for valuable discussion and suggestions during the development of this study. To our colleagues Jodi Rowley, Luis Coloma, Santiago Ron, Alexander Haas, Andreas Nöllert and Brian Gratwicke that kindly provide permission to use the photos included in figure 3, and Paula Acosta who helped with the edition and improving of one of those images.
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