Secondary contact and asymmetrical gene flow in a cosmopolitan marine fish across the Benguela upwelling zone

Abstract

The combination of oceanographic barriers and habitat heterogeneity are known to reduce connectivity and leave specific genetic signatures in the demographic history of marine species. However, barriers to gene flow in the marine environment are almost never impermeable which inevitably allows secondary contact to occur. In this study, eight sampling sites (five along the South African coastline, one each in Angola, Senegal and Portugal) were chosen to examine the population genetic structure and phylogeographic history of the cosmopolitan bluefish (Pomatomus saltatrix), distributed across a large South-east Atlantic upwelling zone. Molecular analyses were applied to mtDNA cytochrome b, intron AM2B1 and 15 microsatellite loci. We detected uncharacteristically high genetic differentiation (F_ST 0.15-0.20; P<0.001) between the fish sampled from South Africa and the other sites, strongly influenced by five outlier microsatellite loci located in conserved intergenic regions. In addition, differentiation among the remaining East Atlantic sites was detected, although mtDNA indicated past isolation with subsequent secondary contact between these East Atlantic populations. We further identified secondary contact, with unidirectional gene flow from South Africa to Angola. The directional contact is likely explained by a combination of the northward flowing offshore current and endogenous incompatibilities restricting integration of certain regions of the genome and limiting gene flow to the south. The results confirm that the dynamic system associated with the Benguela current upwelling zone influences species distributions and population processes in the South-east Atlantic.

Figure 1

(a) Map of oceanographic features and sampling sites of Pomatomus saltatrix in the East Atlantic. Circles indicate sampling sites (Mediterranean—red; Portugal—orange, Senegal—light orange, Angola—yellow, South Africa—green). The arrows indicate the major currents and relative temperature: CC, Canary Current, NEC, North Equatorial Current, ECC, Equatorial Counter Current, GC, Guinea Current, AnC, Angolan Current, SEC, South Equatorial Current, BC, Benguela Current, AgC, Agulhas Current, the light blue shading indicates the upwelling zone at Lüderitz, Namibia. Haplotype networks based on (b) 1039 bp of cytochrome b and (c) 484 bp of AM2B1 with a 95% connection limit, the numbers in the circles represent the number of sequences to provide scale. (d, e) Two clusters were identified as the most likely based on all microsatellites, namely South Africa (SA) and the North East and Central Atlantic (Portugal (POR) and Senegal (SEN) and Angola (ANG, indicated in Orange)) using STRUCTURE 2.3.2. South African sampling sites are indicated in green and consist of Berg River (BR), False Bay (FB), East London (EL), Port Edward (PE) and St Lucia (SL).

Figure 2

Calibrated posterior probability estimates for (a) divergence time in thousands of years (b) effective population size in thousands of individuals (N_E) and (c) the extent and direction of migration (in number of migrations per 1000 of generations per gene copy) across the Benguela upwelling zone estimated in IMa 1.0. Three individual runs (with differing random seeds) are indicated by varying shades of color and are coded as follows: (a) divergence time in shades of black to grey (b) N_E for South Africa in greens, N_E for East Atlantic in oranges and N_E for ancestral populations in greys (c) migration into South Africa in greens and migration into East Atlantic in oranges.