Phylogenetic patterns and the adaptive evolution of osmoregulation in fiddler crabs (Brachyura, Uca)

PLoS One. 2017 Feb 9;12(2):e0171870. doi: 10.1371/journal.pone.0171870. eCollection 2017.

Abstract

Salinity is the primary driver of osmoregulatory evolution in decapods, and may have influenced their diversification into different osmotic niches. In semi-terrestrial crabs, hyper-osmoregulatory ability favors sojourns into burrows and dilute media, and provides a safeguard against hemolymph dilution; hypo-osmoregulatory ability underlies emersion capability and a life more removed from water sources. However, most comparative studies have neglected the roles of the phylogenetic and environmental components of inter-specific physiological variation, hindering evaluation of phylogenetic patterns and the adaptive nature of osmoregulatory evolution. Semi-terrestrial fiddler crabs (Uca) inhabit fresh to hyper-saline waters, with species from the Americas occupying higher intertidal habitats than Indo-west Pacific species mainly found in the low intertidal zone. Here, we characterize numerous osmoregulatory traits in all ten fiddler crabs found along the Atlantic coast of Brazil, and we employ phylogenetic comparative methods using 24 species to test for: (i) similarities of osmoregulatory ability among closely related species; (ii) salinity as a driver of osmoregulatory evolution; (iii) correlation between salt uptake and secretion; and (iv) adaptive peaks in osmoregulatory ability in the high intertidal American lineages. Our findings reveal that osmoregulation in Uca exhibits strong phylogenetic patterns in salt uptake traits. Salinity does not correlate with hyper/hypo-regulatory abilities, but drives hemolymph osmolality at ambient salinities. Osmoregulatory traits have evolved towards three adaptive peaks, revealing a significant contribution of hyper/hypo-regulatory ability in the American clades. Thus, during the evolutionary history of fiddler crabs, salinity has driven some of the osmoregulatory transformations that underpin habitat diversification, although others are apparently constrained phylogenetically.

MeSH terms

  • Animals
  • Biological Evolution*
  • Brachyura / classification
  • Brachyura / genetics*
  • Brachyura / physiology
  • Osmoregulation*
  • Phylogeny*
  • Salt Tolerance*

Grants and funding

This research was supported in Brazil by the Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP fellowships #2008/56305-6 and #2011/08852-0 to SCF, and grants #2007/04870-9 to JCM and #2009/50799-0 to JCM and CLT), the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq #450320/2010-3 and #300662/2009-2 to JCM) and the Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES, 33002029031P8). CLT received funding from the Biology Department, the College of Natural Sciences, and the Graduate College of the University of Northern Iowa, the University of Iowa Global Regional Environmental Research Center (GRERC SA #1000716062, G/P # 1802010001) and the Fulbright Foundation. DBP received post-doctoral fellowships from CNPq (#203734/2014-9) and FAPESP (2016/13949-7). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.