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Unlinking the Speciation Steps: Geographical Factors Drive Changes in Sexual Signals of an Amazonian Nurse-Frog Through Body Size Variation

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Abstract

Geographical and environmental distances influence the divergence of characters among biological populations, especially on a macro spatial scale, making it difficult to interpret the individual contribution of these predictor variables in the process of population differentiation. Anurans are excellent models for multi-character evolutionary studies, due to their low vagility and frequent territoriality, causing certain environmental changes to result in barriers that isolate populations. Accordingly, we propose to test the correlation of environmental and geographical distances in the absence of obvious vicariant barriers with phenotypic and genotypic population characters using, as a study model, an Amazonian litter-frog (Allobates sumtuosus). Combining univariate and multivariate analyses, and Structural Equation Modeling, we tested the general hypotheses that geographical and environmental distances affect the variation in the morphometric, acoustic and genetic characters of this frog along a latitudinal gradient at a fine spatial scale. We found that the latitudinal variation was the most correlated with the variation of the studied characters, with an explanatory force always greater than 78%. Therefore, we suggest that there is a combined effect of latitude and environment on phenotypic characteristics in A. sumtuosus. These factors shape the acoustic characters of this species through pressures on body size, as confirmed by a regression analysis showing that larger body sizes resulted in lower-spectral frequency acoustic signals. This is because the climatic environmental gradient occupied by the species promotes changes in the area-volume relationship of individuals, resulting in larger body sizes towards the Equator. Although we observed a pronounced intrapopulation genetic structure, it was not associated with phenotypic variation. In summary, our study breaks down the stages of speciation for this Amazonian litter-frog, demonstrating that environmental factors lead to changes in the sexual signal due to the variation in body size.

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References

  • Aljanabi, S. M., & Martinez, I. (1997). Universal and rapid salt-extraction of high quality genomic DNA for PCR-based techniques. Nucleic Acids Research, 25(22), 4692–4693.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Amézquita, A., Flechas, S. V., Lima, A. P., et al. (2011). Acoustic interference and recognition space within a complex assemblage of dendrobatid frogs. Proceedings of the National Academy of Sciences, 108(41), 17058–17063.

    Article  Google Scholar 

  • Amézquita, A., Lima, A. P., Jehle, R., et al. (2009). Calls, colours, shape, 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(4), 826–838.

    Article  Google Scholar 

  • Barrett, J. C., Fry, B., Maller, J. D., et al. (2005). Haploview: Analysis and visualization of LD and haplotype maps. Bioinformatics, 21(2), 263–265.

    Article  CAS  PubMed  Google Scholar 

  • Beebee, T. J. C. (2005). Conservation genetics of amphibians. Heredity, 95(6), 423–427.

    Article  CAS  PubMed  Google Scholar 

  • Bevier, C. R., Gomes, F. R., & Navas, C. A. (2008). Variation in call structure and calling behavior in treefrogs of the genus Scinax. South American Journal of Herpetology, 3(3), 196–206.

    Article  Google Scholar 

  • Boul, K. E., Chris Funk, W., Darst, C. R., et al. (2007). Sexual selection drives speciation in an Amazonian frog. Proceedings of the Royal Society B: Biological Sciences, 274(1608), 399–406.

    Article  PubMed  Google Scholar 

  • Charif, R. A., Waack, A. M., & Strickman, L. M. (2010). Raven pro 1.4 user’s manual (p. 25506974). Ithaca, NY: Cornell Lab of Ornithology.

    Google Scholar 

  • Chu, C., Lutz, J. A., Král, K., et al. (2019). Os efeitos diretos e indiretos do clima sobre a riqueza impulsionam o gradiente de diversidade latitudinal nas árvores da floresta. Ecology Letters, 22(2), 245–255.

    PubMed  Google Scholar 

  • Corander, J., & Marttinen, P. (2006). Bayesian identification of admixture events using multilocus molecular markers. Molecular Ecology, 15(10), 2833–2843.

    Article  PubMed  Google Scholar 

  • Corander, J., Marttinen, P., Sirén, J., & Tang, J. (2008). Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinformatics, 9(1), 539.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Cortázar-Chinarro, M., Lattenkamp, E. Z., Meyer-Lucht, Y., et al. (2017). Drift, selection, or migration? Processes affecting genetic differentiation and variation along a latitudinal gradient in an amphibian. BMC Evolutionary Biology, 17(1), 189.

    Article  PubMed  PubMed Central  Google Scholar 

  • Dal Vechio, F., Prates, I., Grazziotin, F. G., et al. (2018). Phylogeography and historical demography of the arboreal pit viper Bothrops bilineatus (Serpentes, Crotalinae) reveal multiple connections between Amazonian and Atlantic rain forests. Journal of Biogeography, 45(10), 2415–2426.

    Article  Google Scholar 

  • de Luna, A. G., Hödl, W., & Amezquita, A. (2010). Colour, size and movement as visual subcomponents in multimodal communication by the frog Allobates femoralis. Animal Behaviour, 79(3), 739–745.

    Article  Google Scholar 

  • De Queiroz, K. (2007). Species concepts and species delimitation. Systematic Biology, 56(6), 879–886.

    Article  PubMed  Google Scholar 

  • Duarte, M. D. O., Freitas, T. M. D. S., & Prudente, A. L. D. C. (2015). Polychromatism of populations of Corallus hortulanus (Squamata: Boidae) from the southern Amazon Basin Brazil. Acta Amazonica, 45(4), 373–382.

    Article  Google Scholar 

  • Ernst, R., & Rödel, M. O. (2008). Patterns of community composition in two tropical tree frog assemblages: Separating spatial structure and environmental effects in disturbed and undisturbed forests. Journal of Tropical Ecology, 24(2), 111–120.

    Article  Google Scholar 

  • Erdtmann, L., & Amézquita, A. (2009). Differential evolution of advertisement call traits in dart-poison frogs (Anura: Dendrobatidae). Ethology, 115(9), 801–811.

    Article  Google Scholar 

  • Erdtmann, L., & Lima, A. P. (2013). Environmental effects on anuran call design: What we know and what we need to know. Ethology Ecology & Evolution, 25(1), 1–11.

    Article  Google Scholar 

  • Ferreira, A. S., Jehle, R., Stow, A. J., & Lima, A. P. (2018). Soil and forest structure predicts large-scale patterns of occurrence and local abundance of a widespread Amazonian frog. Peer J, 6, e5424.

    Article  PubMed  PubMed Central  Google Scholar 

  • Ferreira, A. S., Lima, A. P., Jehle, R., Ferrão, M., & Stow, A. (2020). The influence of environmental variation on the genetic structure of a poison frog distributed across continuous Amazonian rainforest. Journal of Heredity, 111(5), 457–470.

    Article  CAS  Google Scholar 

  • Ficetola, G. F., & Maiorano, L. (2016). Contrasting effects of temperature and precipitation change on amphibian phenology, abundance and performance. Oecologia, 181(3), 683–693.

    Article  PubMed  Google Scholar 

  • Fouquet, A., Gilles, A., Vences, M., et al. (2007). Underestimation of species richness in neotropical frogs revealed by mtDNA analyses. PLoS ONE, 2, 1–10.

    Article  CAS  Google Scholar 

  • Gingras, B., Boeckle, M., Herbst, C. T., & Fitch, W. T. (2013). Call acoustics reflect body size across four clades of anurans. Journal of Zoology, 289(2), 143–150.

    Article  Google Scholar 

  • Hengl, T., de Jesus, J. M., MacMillan, R. A., et al. (2014). soilGrids1km—Global soil information based on automated mapping. PLoS ONE, 9(8), e105992.

    Article  PubMed  PubMed Central  Google Scholar 

  • Hijmans, R. J., Cameron, S. E., Parra, J. L., et al. (2005). Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology, 25(15), 1965–1978.

    Article  Google Scholar 

  • Hijmans, R. J., Van Etten, J., Cheng, J., et al. (2015). Package ‘raster’. R package, 734.

  • Hoskin, C. J., James, S., & Grigg, G. C. (2009). Ecology and taxonomy-driven deviations in the frog call–body size relationship across the diverse Australian frog fauna. Journal of Zoology, 278(1), 36–41.

    Article  Google Scholar 

  • Hurvich, C. M., & Tsai, C. L. (1991). Bias of the corrected AIC criterion for underfitted regression and time series models. Biometrika, 78(3), 499–509.

    Google Scholar 

  • Jaramillo, C., Rand, A. S., Ibáñez, R., & Dudley, R. (1997). Elastic structures in the vocalization apparatus of the tungara frog Physalaemus pustulosus (Leptodactylidae). Journal of morphology, 233(3), 287–295.

    Article  CAS  PubMed  Google Scholar 

  • Jombart, T. (2008). adegenet: A R package for the multivariate analysis of genetic markers. Bioinformatics, 24(11), 1403–1405.

    Article  CAS  PubMed  Google Scholar 

  • Jorge, R. F., Simões, P. I., Magnusson, W. E., & Lima, A. P. (2016). Fine-scale habitat heterogeneity explains the local distribution of two Amazonian frog species of concern for conservation. Biotropica, 48(5), 694–703.

    Article  Google Scholar 

  • Juncá, F. A. (1998). Reproductive biology of Colostethus stepheni and Colostethus marchesianus (Dendrobatidae), with the description of a new anuran mating behavior. Herpetologica, 54, 377–387.

    Google Scholar 

  • Juo, A. S. R., & Franzluebbers, K. (2003). Tropical soils: Properties and management for sustainable agriculture. New York, NY: Oxford University Press.

    Book  Google Scholar 

  • Kaefer, I. L., & Lima, A. P. (2012). Sexual signals of the Amazonian frog Allobates paleovarzensis: Geographic variation and stereotypy of acoustic traits. Behavior, 149(1), 15–33.

    Article  Google Scholar 

  • Kaefer, I. L., Tsuji-Nishikido, B. M., Mota, E. P., et al. (2013). The early stages of speciation in Amazonian forest frogs: Phenotypic conservatism despite strong genetic structure. Evolutionary Biology, 40(2), 228–245.

    Article  Google Scholar 

  • Katoh, K., Rozewicki, J., & Yamada, K. D. (2019). MAFFT online service: Multiple sequence alignment, interactive sequence choice and visualization. Briefings in Bioinformatics, 20(4), 1160–1166.

    Article  CAS  PubMed  Google Scholar 

  • Katoh, K., & Standley, D. M. (2013). MAFFT multiple sequence alignment software version 7: Improvements in performance and usability. Molecular Biology and Evolution, 30(4), 772–780.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kearse, M., Moir, R., Wilson, A., et al. (2012). Geneious basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics, 28(12), 1647–1649.

    Article  PubMed  PubMed Central  Google Scholar 

  • Keller, A., Rödel, M. O., Linsenmair, K. E., et al. (2009). The importance of environmental heterogeneity for species diversity and assemblage structure in Bornean stream frogs. Journal of Animal Ecology, 78(2), 305–314.

    Article  Google Scholar 

  • Kobayashi, S., Abe, S., Tomita, M., et al. (2018). Fine-scale genetic structure and estimation of gene flow of the Japanese brown frog Rana japonica in a Satoyama landscape on the western side of Inba Lake Eastern Japan. Current Herpetology, 37(1), 11–22.

    Article  Google Scholar 

  • Lampert, K. P., Rand, A. S., Mueller, U. G., et al. (2003). Fine-scale genetic pattern and evidence for sex-biased dispersal in the túngara frog Physalaemus pustulosus. Molecular Ecology, 12(12), 3325–3334.

    Article  CAS  PubMed  Google Scholar 

  • Lanfear, R., Frandsen, P. B., Wright, A. M., et al. (2017). PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. Molecular Biology and Evolution, 34(3), 772–773.

    CAS  PubMed  Google Scholar 

  • Leão-Pires, T. A., Luiz, A. M., & Sawaya, R. J. (2018). The complex roles of space and environment in structuring functional, taxonomic and phylogenetic beta diversity of frogs in the Atlantic Forest. PLoS ONE, 13(4), e0196066.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Liao, W., & Lu, X. (2012). Adult body size= f (initial size+ growth rate× age): Explaining the proximate cause of Bergman’s cline in a toad along altitudinal gradients. Evolutionary Ecology, 26(3), 579–590.

    Article  Google Scholar 

  • Liberato, A. M., & Brito, J. I. B. (2010). Influência de mudanças climáticas no balanço hídrico da Amazônia Ocidental. Revista Brasileira de Geografia Física, 3(3), 170–180.

    Article  Google Scholar 

  • Liu, Q., Feng, H., Jin, L., et al. (2018). Latitudinal variation in body size in Fejervarya limnocharis supports the inverse of Bergmann’s rule. Animal Biology, 68(2), 113–128.

    Article  Google Scholar 

  • Maia, G. F., Lima, A. P., & Kaefer, I. L. (2017). Not just the river: Genes, shapes, and sounds reveal population-structured diversification in the Amazonian frog Allobates tapajos (Dendrobatoidea). Biological Journal of the Linnean Society, 121(1), 95–108.

    Article  Google Scholar 

  • Maia-Carvalho, B., Vale, C. G., Sequeira, F., et al. (2018). The roles of allopatric fragmentation and niche divergence in intraspecific lineage diversification in the common midwife toad (Alytes obstetricans). Journal of biogeography, 45(9), 2146–2158.

    Article  Google Scholar 

  • Marchesini, A., Ficetola, G. F., Cornetti, L., et al. (2017). Fine-scale phylogeography of Rana temporaria (Anura: Ranidae) in a putative secondary contact zone in the southern Alps. Biological Journal of the Linnean Society, 122(4), 824–837.

    Article  Google Scholar 

  • Martin WF (1972) Evolution of vocalization in the genus Bufo. Evolution in the genus Bufo, pp 279–309

  • Menin, M., Lima, A. P., Magnusson, W. E., et al. (2007). Topographic and edaphic effects on the distribution of terrestrially reproducing anurans in Central Amazonia: Mesoscale spatial patterns. Journal of Tropical Ecology, 23(5), 539–547.

    Article  Google Scholar 

  • Mitchell, A., & Bergmann, P. J. (2016). Thermal and moisture habitat preferences do not maximize jumping performance in frogs. Functional Ecology, 30(5), 733–742.

    Article  Google Scholar 

  • Montanarin, A., Kaefer, I. L., & Lima, A. P. (2011). Courtship and mating behaviour of the brilliant-thighed frog Allobates femoralis from Central Amazonia: Implications for the study of a species complex. Ethology Ecology & Evolution, 23(2), 141–150.

    Article  Google Scholar 

  • Moraes, L. J. C. L., Pavan, D., Barros, M. C., & Ribas, C. C. (2016). The combined influence of riverine barriers and flooding gradients on biogeographical patterns for amphibians and squamates in south-eastern Amazonia. Journal of Biogeography, 43(11), 2113–2124.

    Article  Google Scholar 

  • Morales, V. (2002). Sistemática y biogeografía del grupo trilineatus (Amphibia, Anura, Dendrobatidae, Colostethus). Publicaciones de La Asociacíon de Amigos de Doñana, 13, 1–59.

    Google Scholar 

  • Morales-Jimenez, A. L., Disotell, T., & Di Fiore, A. (2015). Revisiting the phylogenetic relationships, biogeography, and taxonomy of spider monkeys (genus Ateles) in light of new molecular data. Molecular Phylogenetics and Evolution, 82, 467–483.

    Article  PubMed  Google Scholar 

  • Morton, E. S. (1975). Ecological sources of selection on avian sounds. The American Naturalist, 109(965), 17–34.

    Article  Google Scholar 

  • Mullen, L. M., Vignieri, S. N., Gore, J. A., et al. (2009). Adaptive basis of geographic variation: Genetic, phenotypic and environmental differences among beach mouse populations. Proceedings of the Royal Society B: Biological Sciences, 276(1674), 3809–3818.

    Article  PubMed  PubMed Central  Google Scholar 

  • Naka, L. N., & Brumfield, R. T. (2018). The dual role of Amazonian rivers in the generation and maintenance of avian diversity. Science Advances, 4(8), eaar8575.

    Article  PubMed  PubMed Central  Google Scholar 

  • Newman, R. A., & Squire, T. (2001). Microsatellite variation and fine-scale population structure in the wood frog (Rana sylvatica). Molecular Ecology, 10(5), 1087–1100.

    Article  CAS  PubMed  Google Scholar 

  • Ng, J., Landeen, E. L., Logsdon, R. M., & Glor, R. E. (2013). Correlation between Anolis lizard dewlap phenotype and environmental variation indicates adaptive divergence of a signal important to sexual selection and species recognition. Evolution International Journal of Organic Evolution, 67(2), 573–582.

    Article  PubMed  Google Scholar 

  • Ortiz, D. A., Lima, A. P., & Werneck, F. P. (2018). Environmental transition zone and rivers shape intraspecific population structure and genetic diversity of an Amazonian rain forest tree frog. Evolutionary Ecology, 32(4), 359–378.

    Article  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, MA: Sinauer & Associates Inc.

    Google Scholar 

  • R Core Team (2019) R: A language and environment for statistical com- puting. R Foundation for Statistical Computing

  • Raffel, T. R., Rohr, J. R., Kiesecker, J. M., & Hudson, P. J. (2006). Negative effects of changing temperature on amphibian immunity under field conditions. Functional Ecology, 20(5), 819–828.

    Article  Google Scholar 

  • Rambaut, A., Drummond, A. J., Xie, D., et al. (2018). Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology, 67(5), 901–904.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ribas, C. C., Aleixo, A., Gubili, C., et al. (2018). Biogeography and diversification of Rhegmatorhina (Aves: Thamnophilidae): Implications for the evolution of Amazonian landscapes during the Quaternary. Journal of Biogeography, 45(4), 917–928.

    Article  Google Scholar 

  • Ribeiro, J. E. L. S., Hopkins, M. G., Vicentini, A., et al. (1999). Flora da Reserva Ducke: Guia de Identificação das Plantas Vasculares de uma Floresta de Terra Firme na Amazônia Central. Manaus: INPA.

    Google Scholar 

  • Ronquist, F., Teslenko, M., Van Der Mark, P., et al. (2012). MrBayes 3.2: Efficient Bayesian phylogenetic inference and model choice across a large model space. Systematic Biology, 61(3), 539–542.

    Article  PubMed  PubMed Central  Google Scholar 

  • Rojas, D., Lima, A. P., Momigliano, P., et al. (2019). The evolution of polymorphism in the warning coloration of the Amazonian poison frog Adelphobates galactonotus. Heredity, 124(19), 1–18.

    Google Scholar 

  • Rosseel, Y. (2012). Lavaan: An R package for structural equation modeling and more. Version 0.5–12 (BETA). Journal of Statistical Software, 48(2), 1–36.

    Article  Google Scholar 

  • Simões, P. I., Kaefer, I. L., Farias, I. P., & Lima, A. P. (2013). An integrative appraisal of the diagnosis and distribution of Allobates sumtuosus (Morales, 2002) (Anura, Aromobatidae). Zootaxa, 3746(3), 401–421.

    Article  PubMed  Google Scholar 

  • Simões, P. I., & Lima, A. P. (2012). The tadpole of Allobates sumtuosus (Morales, ‘2000’2002) (Anura: Aromobatidae) from its type locality at Reserva Biológica do Rio Trombetas, Pará Brazil. Zootaxa, 3499(1), 86–88.

    Article  Google Scholar 

  • Simões, P. I., Stow, A., Hödl, W., et al. (2014). The value of including intraspecific measures of biodiversity in environmental impact surveys is highlighted by the Amazonian brilliant-thighed frog (Allobates femoralis). Tropical Conservation Science, 7(4), 811–828.

    Article  Google Scholar 

  • Spurgin, L. G., Illera, J. C., Jorgensen, T. H., et al. (2014). Genetic and phenotypic divergence in an island bird: Isolation by distance, by colonization or by adaptation? Molecular Ecology, 23(5), 1028–1039.

    Article  PubMed  Google Scholar 

  • Stamatakis, A. (2014). RAxML version 8: A tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics, 30(9), 1312–1313.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tryjanowski, P., Sparks, T., Rybacki, M., et al. (2006). Is body size of the water frog Rana esculenta complex responding to climate change? Naturwissenschaften, 93(3), 110–113.

    Article  CAS  PubMed  Google Scholar 

  • Valenzuela-Sánchez, A., Cunningham, A. A., & Soto-Azat, C. (2015). Geographic body size variation in ectotherms: Effects of seasonality on an anuran from the southern temperate forest. Frontiers in Zoology, 12(1), 37.

    Article  PubMed  PubMed Central  Google Scholar 

  • van Rensburg AJ, Cortazar-Chinarro M, Laurila A et al (2018). Adaptive genomic variation associated with environmental gradients along a latitudinal cline in Rana temporaria. biorxiv 427872

  • Vences, M., Thomas, M., Van der Meijden, A., et al. (2005). Comparative performance of the 16S rRNA gene in DNA barcoding of amphibians. Frontiers in Zoology, 2(1), 5.

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Zeisset, I., & Beebee, T. J. C. (2008). Amphibian phylogeography: A model for understanding historical aspects of species distributions. Heredity, 101(2), 109–119.

    Article  CAS  PubMed  Google Scholar 

  • Zimmerman, B. L., & Bierregaard, R. (1986). Relevance of the equilibrium theory of island biogeography and species-area relations to conservation with a case from Amazonia. Journal of Biogeography, 13(2), 133–143.

    Article  Google Scholar 

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Acknowledgements

We are grateful to the National Council for Scientific and Technological Development (CNPq) for the financial support through productivity grants to MM, IPF, APL and ILK; and a research grant (Universal 405640/2016-1) for MM. The Amazon Research Support Foundation (FAPEAM) for the master's scholarship to IYF. The Coordination for the Improvement of Higher Education Personnel (CAPES) for financial support and the Graduate Program in Ecology (PPG-Eco INPA) for structural and logistical support. Specimens were collected under collection permit 67501-2 provided by the Chico Mendes Institute for Biodiversity Conservation (ICMBio).

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Fernandes, I.Y., Moraes, L.J.C.L., Menin, M. et al. Unlinking the Speciation Steps: Geographical Factors Drive Changes in Sexual Signals of an Amazonian Nurse-Frog Through Body Size Variation. Evol Biol 48, 81–93 (2021). https://doi.org/10.1007/s11692-020-09525-7

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