Ecological opportunities and specializations shaped genetic divergence in a highly mobile marine top predator

Abstract

Environmental conditions can shape genetic and morphological divergence. Release of new habitats during historical environmental changes was a major driver of evolutionary diversification. Here, forces shaping population structure and ecotype differentiation ('pelagic' and 'coastal') of bottlenose dolphins in the North-east Atlantic were investigated using complementary evolutionary and ecological approaches. Inference of population demographic history using approximate Bayesian computation indicated that coastal populations were likely founded by the Atlantic pelagic population after the Last Glacial Maxima probably as a result of newly available coastal ecological niches. Pelagic dolphins from the Atlantic and the Mediterranean Sea likely diverged during a period of high productivity in the Mediterranean Sea. Genetic differentiation between coastal and pelagic ecotypes may be maintained by niche specializations, as indicated by stable isotope and stomach content analyses, and social behaviour. The two ecotypes were only weakly morphologically segregated in contrast to other parts of the World Ocean. This may be linked to weak contrasts between coastal and pelagic habitats and/or a relatively recent divergence. We suggest that ecological opportunity to specialize is a major driver of genetic and morphological divergence. Combining genetic, ecological and morphological approaches is essential to understanding the population structure of mobile and cryptic species.

Isotopic niches of fin whales from the Mediterranean Sea and the Celtic Sea (North Atlantic)

“…During the last glacial maximum (from 26,500 to 19,000 years ago (Clark, 2009)), habitat conditions in the Mediterranean Sea were strikingly different from the current oligotrophic state, with colder conditions (Fontaine et al, 2014(Fontaine et al, , 2010. The Mediterranean Sea was a suitable habitat for cold-water species such as the harbour porpoise (Fontaine et al, 2014(Fontaine et al, , 2010. The postglacial warming presumably led to habitat fragmentation and eventually to the retreat of the harbour porpoise from most of the Mediterranean Sea (Cucknell et al, 2016;Fontaine et al, 2014Fontaine et al, , 2010.…”

“…Indeed this is already occurring for baleen whales in the western North Atlantic (Ramp et al, 2015). During the last glacial maximum (from 26,500 to 19,000 years ago (Clark, 2009)), habitat conditions in the Mediterranean Sea were strikingly different from the current oligotrophic state, with colder conditions (Fontaine et al, 2014(Fontaine et al, , 2010. The Mediterranean Sea was a suitable habitat for cold-water species such as the harbour porpoise (Fontaine et al, 2014(Fontaine et al, , 2010.…”

“…The Mediterranean Sea was a suitable habitat for cold-water species such as the harbour porpoise (Fontaine et al, 2014(Fontaine et al, , 2010. The postglacial warming presumably led to habitat fragmentation and eventually to the retreat of the harbour porpoise from most of the Mediterranean Sea (Cucknell et al, 2016;Fontaine et al, 2014Fontaine et al, , 2010. The study of the genetic isolation process of the fin whale from the Mediterranean Sea from its Atlantic counterpart is yet to be investigated but a similar continuum of events could be envisaged.…”

“…Niche variation owing to individual differences in ecology has been hypothesized to be an early stage of sympatric speciation (Foote et al, 2013). Environmental variation is a major driver of evolutionary divergence (Louis et al, 2014). It can lead to natural selection on environment-associated traits, limiting gene flow and facilitating local adaptation of ecologically distinct groups of individuals (Kawecki and Ebert, 2004;Schluter, 2001).…”

“…, 1981, 1978). Contribution of each assimilated prey source are proportionally reflected in the tissues of a predator, after accounting for isotopic fractionation in the digestion and assimilation process Epstein, 1981, 1978 consumer is therefore close to that of the diet and is typically used to indicate relative contributions to the diet of different potential primary producers in a trophic network, indicating for example the aquatic vs. terrestrial, inshore vs. offshore or pelagic vs. benthic contribution to food intake (Louis et al, 2014;Smith et al, 1996).…”