Patterns of genetic isolation in a widely distributed pelagic fish, the narrow-barred Spanish mackerel (Scomberomorus commerson)

Abstract

Although migratory pelagic fishes generally exhibit little geographic differentiation across oceans, as expected from their life-history (broadcast spawning, pelagic larval life, swimming ability of adults) and the assumed homogeneity of the pelagic habitat, exceptions to the rule deserve scrutiny. One such exception is the narrow-barred Spanish mackerel (Scomberomorus commerson), where strong genetic heterogeneity at the regional scale has been previously reported. We investigated the genetic composition of S. commerson across the Indo-West Pacific range using control-region sequences (including previously published datasets), cytochrome-b gene partial sequences, and eight microsatellite loci, to further explore its phylogeographic structure. All haplotypes sampled from the Indo-Malay-Papua archipelago (IMPA) and the southwestern Pacific coalesced into a clade (Clade II) that was deeply separated (14.5% nucleotide divergence) from a clade grouping all haplotypes from the Persian Gulf and Oman Sea (Clade I). Such a high level of genetic divergence suggested the occurrence of two sister-species. Further phylogeographic partition was evident between the western IMPA and the regions sampled east and south of it, i.e. northern Australia, West Papua, and the Coral Sea. Strong allele-frequency differences were found between local populations in the southwestern Pacific, both at the mitochondrial locus (ΦST=0.282-0.609) and at microsatellite loci (^θ=0.202-0.313). Clade II consisted of four deeply divergent subclades (9.0-11.8% nucleotide divergence for the control region; 0.3-2.5% divergence at the cytochrome b locus). Mitochondrial sub-clades within Clade II generally had narrow geographic distribution, demonstrating further genetic isolation. However, one particular haplogroup within Clade II was present throughout the central Indo-West Pacific; that haplogroup was found to be sister-group to an haplogroup restricted to West Papua and the Coral Sea, yielding evidence of recent secondary westward colonization. Such a complex structure is in sharp contrast with the generally weak phylogeographic patterns uncovered to date in other widely distributed, large pelagic fishes with pelagic eggs and larvae. We hypothesize that in S. commerson and possibly other Scomberomorus species, philopatric migration may play a role in maintaining the geographic isolation of populations by annihilating the potential consequences of passive dispersal.