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Salinity tolerance explains the contrasting phylogeographic patterns of two swimming crabs species along the tropical western Atlantic

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Abstract

Patterns and processes of species diversification in the oceans are still not fully understood. Traditionally, studies have been using the pelagic larval duration (PLD) to explain the genetic structure and phylogeographic history of marine taxa. However, this trait has given inconsistent results, especially when there is a physiological barrier. Phylogeographic studies comparing species that have similar PLD but differ in other important traits can indicate which ones drive intraspecific evolution. To test our hypothesis, we selected two species with similar distribution and PLD and different salinity tolerance to explore the role of Amazon-Orinoco plume (the biggest freshwater discharge into the ocean worldwide) in the diversification of western Atlantic species. We amplified mtDNA markers (COI and 16S rRNA) of Callinectes ornatus (less tolerant to low salinity) and C. danae (tolerant to low salinity) from both sides of the Amazon-Orinoco plume (four biogeographical provinces). Then, we performed genetic structure, historical demography, divergence time, and biogeographic modelling analyses. Our results show contrasting phylogeographic and demographic patterns that can be explained by salinity tolerance. The Amazon-Orinoco plume represents a barrier for C. ornatus, which has two evolutionary units (ESUs). The plume is not a barrier for C. danae, which has no genetic structure. Furthermore, C. ornatus is formed by an ancestral Caribbean group that dispersed to the southwestern Atlantic after the establishment of the Amazon-Orinoco plume. Callinectes danae has undergone demographic changes during the Last Glacial Maximum, probably due to the loss of estuarine habitats due to sea level fall, while C. ornatus was not affected because it is absent in this type of environment. Therefore, we show that ecological traits of marine taxa, like salinity tolerance, are more reliable predictors of genetic variation than the usually used larval dispersal potential.

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Acknowledgements

This research is resulted from the PhD project of Pedro A. Peres supported by São Paulo Research Foundation—FAPESP by a scholarship (2017/12376-6). All financial support was provided by grants from FAPESP (Temático Biota 2010/50188-8 and Biota INTERCRUSTA 2018/13685-5; Coleções Científicas 2009/54931-0; PROTAX 2016/50376-5), Conselho Nacional de Desenvolvimento Científico e Tecnológico—CNPq (301359/2007-5; 473050/2007-2; 302748/2010-5; 471011/2011-8; PQ 302253/2019-0), and Coordenação de Aperfeiçoamento de Pessoal—CAPES—Código de Financiamento 001 (Ciências do Mar II—2005/2014–23038.004308/201414) granted to FLM. We are grateful to Gustav Paulay and John Slapcinsky (FLMNH), Cleverson Santos (MPEG) and all the colleagues of the Laboratory of Bioecology and Crustacean Systematics (LBSC) for their help with sampling, donation and lending specimens used herein. We are also grateful to Dr. Heather Bracken-Grissom for suggested improvements to the manuscript, to anonymous reviewers and editors for their suggestions and corrections that improved the manuscript during review process. The collections of species conducted in this study complied with current applicable state and federal laws of Brazil (permanent license to FLM for collection of Zoological Material No. 11777-1 MMA/IBAMA/SISBIO). The authors declare no conflicts of interest.

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  1. Laboratory of Bioecology and Crustacean Systematics (LBSC), Graduate Program in Comparative Biology, Department of Biology, Faculty of Philosophy, Sciences and Letters at Ribeirão Preto (FFCLRP), University of São Paulo (USP), Av. Bandeirantes 3900, Ribeirão Preto, São Paulo, 14040-901, Brazil

    Pedro A. Peres & Fernando L. Mantelatto

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  1. Pedro A. Peres
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PAP: Conceptualization, Methodology, Formal analysis and Investigation, Writing – original draft, Writing – review and editing. FLM: Conceptualization, Writing – review and editing, Funding acquisition, Resources, Supervision.

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Correspondence to Pedro A. Peres.

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Peres, P.A., Mantelatto, F.L. Salinity tolerance explains the contrasting phylogeographic patterns of two swimming crabs species along the tropical western Atlantic. Evol Ecol 34, 589–609 (2020). https://doi.org/10.1007/s10682-020-10057-x

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