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

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.

The chicken or the egg? Adaptation to desiccation and salinity tolerance in a lineage of water beetles

“…According to the ancestral reconstruction of habitat salinity, neither E. testaceus nor E. politus had saline ancestors, something that is only compatible with the first of our proposed hypotheses, that is, that hyporegulation ability was co‐opted from desiccation resistance mechanisms. A lack of association between habitat salinity and osmoregulatory ability has also been reported in some crustaceans (e.g., Faria et al., ; McNamara & Faria, ). Grapsid and ocypodid crabs present an example of how selection on mechanisms to reduce water loss under aerial desiccation (gill function in this case) indirectly has improved underwater osmoregulation ability, meaning desiccation resistance and osmoregulation capacities are positively associated (Faria et al., ; Takeda, Matsumasa, Kikuchi, Poovachiranon, & Murai, ).…”

“…A lack of association between habitat salinity and osmoregulatory ability has also been reported in some crustaceans (e.g., Faria et al., ; McNamara & Faria, ). Grapsid and ocypodid crabs present an example of how selection on mechanisms to reduce water loss under aerial desiccation (gill function in this case) indirectly has improved underwater osmoregulation ability, meaning desiccation resistance and osmoregulation capacities are positively associated (Faria et al., ; Takeda, Matsumasa, Kikuchi, Poovachiranon, & Murai, ). In the case of water beetles, selection on mechanisms such as those involved in ion transport, cell volume regulation or cuticle permeability for the control of water loss under desiccation might have resulted in enhanced hyporegulation ability.…”

“…In general, species of Lumetus (and other beetle genera) typical of hypersaline waters are almost absent from freshwater habitats, despite been able to hyper‐regulate (Céspedes et al., ; Pallarés et al., ; Tones, )—although E. bicolor is regularly found in low mineralized waters in northern localities of Europe. Such a situation also holds for saline Hemiptera (corixids, Tones & Hammer, ), coastal and estuarine decapods (Faria et al., ; McNamara & Faria, ) and fish (Schultz & McCormick, ). The maintenance of hyper‐regulation ability despite the apparent loss of its ecological role may reflect positive pleiotropies or functional correlations between hypo‐ and hyper‐regulatory mechanisms (e.g., Smith, VanEkeris, Okech, Harvey, & Linser, ; Smith, Raymond, Valenti, Smith, & Linser, ), but may also be just due to the low cost of maintaining functional osmoregulatory responses outside conditions commonly encountered in nature (Divino et al., ).…”

“…All species were exposed to at least two common hyposmotic treatments (0.3 and 12 g/L) and a hyperosmotic one (35 g/L) to obtain comparable osmolality measurements. For each species, the treatment in which mortality exceeded 50% of the tested individuals was considered as the upper lethal limit (e.g., Faria et al., ) (Table ). From each treatment, we obtained haemolymph samples from a minimum of three of the exposed individuals (Table ), as pilot trails showed low intraspecific variation within salinity treatments.…”

“…The relationship between tolerance to salinity and desiccation has been mostly studied in plants (e.g., Barrieu et al, 1999;Cayuela et al, 2007;Hossain, Mostofa, & Fujita, 2013) and to a lesser extent in animal taxa (Faria, Provete, Thurman, & McNamara, 2017;G omez-Mestre & Tejedo, 2005). Despite the relevance of such relationship, to our knowledge, no previous studies have addressed the potential evolutionary links between mechanisms to deal with salinity and desiccation.…”