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.

Keywords: bottlenose dolphins; demographic history; ecological niches; morphology; population genetics.

Figure 1.

Sample locations and genetic populations of bottlenose dolphins included in demographic history analyses.

Figure 2.

Schematic diagram of hierarchical ABC analysis to compare various evolutionary histories and divergence scenarios generated and tested using the program DIYABC. PM, Pelagic Mediterranean; PA, Pelagic Atlantic; CS, Coastal South; CN, Coastal North.

Figure 3.

Skin δ³⁴S and δ¹⁵N values for genetically determined coastal and pelagic bottlenose dolphins. Solid lines indicate SEA_C and dotted lines convex hull areas. Their respective areas values (‰²) are given in the legend. Asterisk indicates the possible migrant (see text). (Online version in colour.)

Figure 4.

Bar graph of individual assignment probabilities to each of the two isotopic clusters and comparison with genetic groups. Each vertical bar represents one individual. Asterisk indicates the possible migrant (see text). (Online version in colour.)