The Early Stages of Speciation in Amazonian Forest Frogs: Phenotypic Conservatism Despite Strong Genetic Structure
- 648 Downloads
Phylogeographic perspectives incorporating multiple classes of characters, especially those relating to sexual signals, are promising for the elucidation of recent evolutionary mechanisms driving speciation. Here, forest frogs were used as a model system to access distinct stages in the process of evolutionary differentiation. We studied 280 individuals assigned to three species: Allobates paleovarzensis, A. nidicola and A. masniger. Samples were collected at 20 localities arranged in two study systems, along the middle Amazon and the lower Madeira Rivers, in Central Amazonia. Mantel tests, analyses of molecular variance, and the spatial distribution of haplogroups indicated that the distribution of genetic variability, as inferred from a mitochondrial DNA marker, was determined by a combination of isolation-by-distance effects and the transposition of large Amazonian rivers. These two factors had contrasting relative influences in each of the study systems, which also differed regarding the estimated time of the major cladogenetic events. Pronounced population genetic structure was observed. However, multivariate discriminant function analyses revealed that the phenotypic (morphological and acoustic) divergence was loosely related with genetic differentiation and did not successfully predict assignment of individuals to genetic groups. The observed distribution of genetic variability showed the important role of genetic drift in the diversification of the mitochondrial marker studied. The phenotypic conservatism among populations was surprising in view of the high genetic structuring observed, and indicates a prevailing role of stabilizing selective forces in the process of sexual signal and morphological differentiation.
KeywordsGenetic drift Integrative phylogeography Isolation by distance Mitochondrial DNA River barrier Sexual signals
We thank Anelise Montanarin, Francisco C. de Freitas, Irene da S. Melo, Maria A. Carvalho, Moisés da S. Melo and Raimundo N. Amorim for fieldwork assistance; Daniela Leroy e Waleska Gravena for help in laboratory procedures; Adolfo Amézquita, Adrian Garda, Andrew J. Crawford, Camila Ribas, Heike Pröhl, Janet W. Reid, Jeffrey Podos, Luciana K. Erdtmann, Marcelo Gordo, Marcelo Menin, Marina Anciães, Pedro Ivo Simões, Tomas Hrbek, Vanessa Verdade and Walter Hödl for valuable suggestions during this study. We extend thanks to two anonymous reviewers whose observations led to further improvements in the text. We also thank the Brazilian Conselho de Desenvolvimento Científico e Tecnológico for financial support (CNPq-CT Amazônia 553997/2006-8 and 575572/2008-6).
Conflict of interest
The authors declare that they have no conflict of interest.
This study complies with the current Brazilian laws and was allowed by RAN-ICMBio/IBAMA (licences 13777-2, 18516-1, 20065-2, and 21950-1).
- Amézquita, A., Lima, A. P., Jehle, R., Castellanos, L., Ramos, O., Crawford, A. J., et al. (2009). Calls, colours, shapes, and genes: A multi–trait approach to the study of geographic variation in the Amazonian frog Allobates femoralis. Biological Journal of the Linnean Society, 98, 826–838.CrossRefGoogle Scholar
- Angulo, A., & Reichle, S. (2008). Acoustic signals, species diagnosis, and species concepts: The case of a new cryptic species of Leptodactylus (Amphibia, Anura, Leptodactylidae) from the Chapare region, Bolivia. Zoological Journal of the Linnean Society, 152, 58–77.Google Scholar
- Antonelli, A., Quijada-Mascareñas, A., Crawford, A. J., Bates, J. M., Velazco, P. M., & Wüster, W. (2010). Molecular studies and phylogeography of Amazonian tetrapods and their relation to geological and climatic models. In C. Hoorn & F. P. Wesselingh (Eds.), Amazonia, landscape and species evolution (pp. 386–403). Oxford: Blackwell Publishing.Google Scholar
- Avise, J. C. (2000). Phylogeography: The history and formation of species. Cambridge: Harvard University Press.Google Scholar
- Avise, J. C. (2004). Molecular markers, natural history and evolution (2nd ed.). Sunderland: Sinauer Associates Inc.Google Scholar
- Bonnet, E., & Van de Peer, Y. (2002). ZT: A software tool for simple and partial Mantel tests. Journal of Statistical Software, 7, 1–12.Google Scholar
- Capparella, A. P. (1988). Genetic variation in Neotropical birds: Implications for the speciation process. In H. Ouellet (Ed.), Acta XIX Congressus Internationalis Ornithologici (pp. 1658–1664). Ottawa: University of Ottawa Press.Google Scholar
- Charif, R. A., Clark, C. W., & Fristrup, K. M. (2004). Raven 1.2 User’s manual. Ithaca: Cornell Laboratory of Ornithology.Google Scholar
- Charif, R. A., Waack, A. M., & Strickman, L. M. (2008). Raven Pro 1.3 User’s manual. Ithaca: Cornell Laboratory of Ornithology.Google Scholar
- Cohn-Haft, M. (2000). A case study in amazonian biogeography: Vocal and DNA sequence variation in Hemitriccus flycatchers. PhD thesis. Luisiana State University.Google Scholar
- Coyne, J. A., & Orr, H. A. (2004). Speciation. Sunderland: Sinauer Associates Inc.Google Scholar
- Crisci, J. V., Katinas, L., & Posadas, P. (2003). Historical biogeography: An introduction. Cambridge: Harvard University Press.Google Scholar
- Fouquet, A., Recoder, R., Teixeira, M., Jr, Cassimiro, J., Amaro, R. C., Camacho, A., et al. (2012b). Molecular phylogeny and morphometric analyses reveal deep divergence between Amazonia and Atlantic Forest species of Dendrophryniscus. Molecular Phylogenetics and Evolution, 62, 826–838.PubMedCrossRefGoogle Scholar
- Gerhardt, H. C., & Huber, F. (2002). Acoustic communication in insects and anurans: Common problems and diverse solutions. Chicago: University of Chicago Press.Google Scholar
- Hall, T. A. (1999). BioEdit: A user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symposium Series, 41, 95–98.Google Scholar
- Irion, G., & Kalliola, R. (2010). Long–term landscape development processes in Amazonia. In C. Hoorn & F. P. Wesselingh (Eds.), Amazonia, landscape and species evolution (pp. 185–197). Oxford: Blackwell Publishing.Google Scholar
- Kaefer, I. L., Montanarin, A., Costa, R. S., & Lima, A. P. (in press). Temporal patterns of reproductive activity and site attachment of the Brilliant–thighed Frog Allobates femoralis from Central Amazonia. Journal of Herpetology.Google Scholar
- Lima, A. P., Caldwell, J. P., Biavati, G., & Montanarin, A. (2010). A new species of Allobates (Anura: Aromobatidae) from paleovárzea forest in Amazonas, Brazil. Zootaxa, 2337, 1–17.Google Scholar
- Morales, V. R. (2002). Sistematica y biogeografía del grupo trilineatus (Amphibia, Anura, Dendrobatidae, Colostethus), con descripción de once nuevas especies. Publicación de la Asociación Amigos Doñana, 13, 1–59.Google Scholar
- Palumbi, S. R. (1996). Nucleic acids II: the polymerase chain reaction. In D. M. Hillis, C. Moritz, & B. K. Mable (Eds.), Molecular systematics (pp. 205–247). Sunderland: Sinauer Associates Inc.Google Scholar
- Rambaut, A., & Drummond, A. J. (2007). Tracer v. 1.5. [http://beast.bio.ed.ac.uk/Tracer]. Accessed 04 May 2012.
- Santos, S., Hrbek, T., Farias, I. P., Schneider, H., & Sampaio, I. (2006). Population genetic structuring of the king weakfish, Macrodon ancylodon (Sciaenidae), in Atlantic coastal waters of South America: Deep genetic divergence without morphological change. Molecular Ecology, 15, 4361–4373.PubMedCrossRefGoogle Scholar
- Sequeira, F., Sodré, D., Ferrand, N., Bernardi, J., Sampaio, I., Schneider, H., et al. (2011). Hybridization and massive mtDNA unidirectional introgression between the closely related Neotropical toads Rhinella marina and R. schneideri inferred from mtDNA and nuclear markers. BMC Evolutionary Biology, 11, 264.PubMedCrossRefGoogle Scholar
- Simões, P. I. (2010). Diversificação do complexo Allobates femoralis (Anura, Dendrobatidae) em florestas da Amazônia brasileira: desvendando padrões atuais e históricos. PhD thesis. Manaus: Instituto Nacional de Pesquisas da Amazônia.Google Scholar
- Sioli, H. (1984). The Amazon: Limnology and landscape ecology of a mighty tropical river and its basin. Dordrecht: Dr W. Junk Publisher.Google Scholar
- Tsuji-Nishikido, B. M., Kaefer, I. L., Freitas, F. C., Menin, M., & Lima, A. P. (2012). Significant but not diagnostic: Differentiation through morphology and calls in the Amazonian frogs Allobates nidicola and A. masniger. Herpetological Journal, 22, 105–114.Google Scholar
- Vences, M., Kosuch, J., Lötters, S., Widmer, A., Jungfer, K., Köhler, J., et al. (2000). Phylogeny and classification of Poison Frogs (Amphibia: Dendrobatidae), based on mitochondrial 16S and 12S ribosomal RNA gene sequences. Molecular Phylogenetics and Evolution, 15, 34–40.PubMedCrossRefGoogle Scholar
- Vences, M., & Wake, D. B. (2007). Speciation, species boundaries and phylogeography of amphibians. In H. H. Heatwole & M. Tyler (Eds.), Amphibian biology. Volume 6: Systematics (pp. 2613–2669). Chipping Norton: Surrey Beatty & Sons.Google Scholar
- Wallace, A. R. (1852). On the monkeys of the Amazon. Proceedings of the Zoological Society of London, 20, 107–110.Google Scholar
- Wright, S. (1951). The genetical structure of populations. Annals of Human Genetics, 15, 323–354.Google Scholar