Biogeography and temporal progression during the evolution of striped dolphin population structure in European waters

Abstract

Aim We investigated the population genetic structure of a highly mobile marine species, the striped dolphin, Stenella coeruleoalba (Meyen, 1833), along a geographical range with habitat transitions and historical dynamics to identify the causes of genetic divergence, and to assess the effect of past climate change on demography and population connectivity. Location North‐east Atlantic Ocean and Mediterranean Sea. Methods Twenty microsatellite loci were used in conjunction with coalescent methods to investigate the genetic structure and demographic history of striped dolphins (Stenella coeruleoalba) in the Mediterranean Sea and eastern North Atlantic Ocean. Approximate Bayesian modelling was used to compare the support for alternative scenarios for the pattern of divergence over time in the context of known geographical transitions and environmental change over the course of the Quaternary. Results We describe a novel pattern of structure among the extant populations along north–south and east–west axes. Modern gene flow shows strong directionality from north‐east to south and west in the North Atlantic, and from west to east in the Mediterranean. On a temporal scale we found evidence for a progression starting with a division between the North Atlantic and Mediterranean Sea populations during the middle Pleistocene, followed by a division within the Mediterranean between the east and west basins towards the end of the Pleistocene, and finally an east–west division in the eastern North Atlantic at the start of the Holocene. Main conclusions In the context of known population structure for other marine species along the same geographical range, our data facilitate inference of the more general processes that shaped patterns of biogeography across this region through the environmental transitions of the Quaternary. In particular, Pleistocene era divisions apparently reflect strong physical habitat boundaries, with later divisions associated with climate warming in the Holocene.

Spatio-temporal patterns of genetic diversity in the Mediterranean striped dolphin (Stenella coeruleoalba)

“…However, no strong geographic population structure was found in our fairly comprehensive analysis across the Mediterranean Sea. Although this pattern is apparently in contrast with suggestions from previous studies (Gaspari et al., ; Gkafas et al., ), several features in our data could potentially account for the apparent discordance. First, nuclear loci show significant F ST levels between many of the Mediterranean Sea basins identified (Table ).…”

“…Geographic structure between the Mediterranean basin and the northeast Atlantic was identified, consistent with previous studies (Bourret et al., ; Garcia‐Martinez et al., ; Gaspari et al., ; Gkafas et al., ). However, no strong geographic population structure was found in our fairly comprehensive analysis across the Mediterranean Sea.…”

“…Simultaneously, reduced density after a mortality event could lead to episodes of immigration (as suggested previously; Gkafas et al., ), which would not be easily detected in genetic patterns if migrant individuals and/or F1 hybrids are not sampled, but could originate individuals with shared genetic ancestry across regions (as found in this study). This could suggest that epizootics result from an increase in the density of susceptible individuals, both due to population growth, as juveniles quickly lose their maternal immunity (Van Bressem et al., ), and/or immigrants which would have not been previously exposed to the virus.…”

“…Population genetic summary statistics were calculated for microsatellite genotypes between 1987 and 2009, using a sliding window of 3‐year and 1‐year steps (samples from outside the Mediterranean were not included, because of the known patterns of genetic differentiation between the Atlantic and the Mediterranean; Garcia‐Martinez et al., ; Bourret et al., ; Gaspari et al., ; Gkafas et al., ). This strategy was adopted for three main reasons: Sampling size was uneven between years, so pooling ensured statistical tests and descriptors were based on large enough sample sizes.…”

“…The striped dolphin is the most common cetacean in the Mediterranean Sea (Gaspari, Azzelino, Airoldi, & Hoelzel, ). Previous studies suggest that striped dolphins in the Mediterranean basin are genetically differentiated from the Atlantic Ocean (Bourret, Macé, & Crouau‐Roy, ; Garcia‐Martinez, Moya, Raga, & Latorre, ; Gaspari et al., ), with further subdivision within the Mediterranean Sea being suggested by kinship analysis (Gaspari et al., ) and factorial analyses (Gkafas et al., ). Furthermore, in the last three decades the striped dolphin has faced ecological pressure from a series of morbillivirus epizootics across the Mediterranean basin (Di Guardo & Mazzariol, ).…”