Colonisation of toxic environments drives predictable life‐history evolution in livebearing fishes (Poeciliidae)

Abstract

New World livebearing fishes (family Poeciliidae) have repeatedly colonised toxic, hydrogen sulphide-rich waters across their natural distribution. Physiological considerations and life-history theory predict that these adverse conditions should favour the evolution of larger offspring. Here, we examined nine poeciliid species that independently colonised toxic environments, and show that these fishes have indeed repeatedly evolved much larger offspring size at birth in sulphidic waters, thus uncovering a widespread pattern of predictable evolution. However, a second pattern, only indirectly predicted by theory, proved additionally common: a reduction in the number of offspring carried per clutch (i.e. lower fecundity). Our analyses reveal that this secondary pattern represents a mere consequence of a classic life-history trade-off combined with strong selection on offspring size alone. With such strong natural selection in extreme environments, extremophile organisms may commonly exhibit multivariate phenotypic shifts even though not all diverging traits necessarily represent adaptations to the extreme conditions.

Speciation in Freshwater Fishes

“…Well-studied cases are those in livebearers of the genera Poecilia and Gambusia inhabiting sulfidic versus freshwater streams and caves in Mexico and the Caribbean. Multiple cases of early and advanced incipient speciation and some cases of older speciation events, both parapatric and allopatric, have been demonstrated in both genera (Palacios et al 2013, Riesch et al 2014, associated with strong but asymmetric divergent selection between and adaptation to sulfidic and hypoxic waters versus normoxic freshwaters.…”

Patterns of Macroinvertebrate and Fish Diversity in Freshwater Sulphide Springs

“…Most phenotypic traits investigated show strong signals of convergent evolution in evolutionarily independent lineages of Poecilia as well as other poeciliid taxa investigated to date [71,74,76,77].…”

“…For example, the presence of H 2 S affects energy budgets of sulphide spring residents, both because sulphide detoxification is energetically costly and energy acquisition is constrained by aquatic surface respiration [125]. As a consequence, some sulphide spring Poecilia are in worse nutritional condition [132] (see [71]), exhibit changes in energy metabolism [133], and diverged in life history strategies, producing fewer but substantially larger offspring [71,74,134]. In addition, colonizing sulphide springs was accompanied by changes in trophic resource use, where Poecilia switched from a typically algivorous diet in non-sulphidic habitats to a diet consisting of sulphur-metabolizing bacteria and invertebrates in sulphidic habitats [94,131].…”

Full Issue

“…This spatial and temporal variance in selection pressures is likely the underlying cause of observed egg-size variation between and within species (Fox and Czesak 2000). Recently, this hypothesis was supported in several fish species (Einum and Fleming 1999, Bashey 2008, Rollinson and Hutchings 2013, Riesch et al 2014.…”