Highly restricted gene flow between disjunct populations of the skunk clownfish (Amphiprion akallopisos) in the Indian Ocean

Abstract

The skunk clownfish (Amphiprion akallopisos) has a disjunct distribution, occurring in the Eastern Indian Ocean (EIO) and the Western Indian Ocean (WIO), separated by several thousands of kilometres. Information on connectivity of marine species is very important for the correct spacing of marine protected areas, a powerful instrument for the protection of coral reefs. The population genetic structure of A. akallopisos was analysed in order to investigate connectivity amongst populations and to explain the disjunct distribution of the species. A fragment of the mitochondrial control region was used to investigate the genetic population structure. Fin clips were collected from 263 individuals at 14 sites in the WIO and three sites in the EIO. The obtained DNA sequences were used to calculate genetic diversity, evaluate demographic history and to construct a haplotype network. An analysis of molecular variance (AMOVA) was conducted to evaluate the significance of the observed genetic population structure. None of the identified 69 haplotypes was shared between the WIO and EIO. Haplotype as well as nucleotide diversity was considerably higher in the EIO than in the WIO. Significant genetic population structure was revealed by an AMOVA with an overall φst‐value of 0.28 (P < 0.001) in the Indian Ocean. The overall AMOVA (φst = −0.00652) was not significant in the EIO, but was significant in the WIO (φst = 0.016; P < 0.01). Demographic analysis indicated population expansion in the EIO and WIO. Population genetic analysis revealed highly restricted gene flow between the EIO and WIO. Genetic diversity was much higher in the EIO than in the WIO, suggesting that the EIO is the geographical origin of the species. Given the large distance between the disjunct populations and the short pelagic larval duration, long‐distance dispersal is rather unlikely. A stepping stone model involving islands in the Central Indian Ocean is a more likely scenario for colonization of the WIO.

Genetic Population Structure of the Coral Reef Sea Star Linckia laevigata in the Western Indian Ocean and Indo-West Pacific

“…The first hierarchical grouping shows that the WIO populations are genetically distinct from the EIO populations, suggesting a WIO-EIO divide. This break within the Indian Ocean was also observed in the giant clams Tridacna maxima and Tridacna squamosa [73], the anemonefish Amphiprion akallopisos [58], the crown-of-thorns sea star Acanthaster planci [74], and the black tiger prawn Penaeus monodon [50, 66]. The limited genetic exchange between the WIO and EIO supports the notion that fewer islands exist in the Indian Ocean compared to the West Pacific in order to facilitate dispersal through “island hopping”.…”

“…Population expansion after a population bottleneck has also been observed in the IMPA populations of L . laevigata [14, 34, 57] and in other species in the WIO, such as the anemonefish Amphiprion akallopisos [58], mangrove crab Neosarmatium meinerti [53], fiddler crab Uca annulipes [51], mud crab Scylla serrata [59], and giant tiger prawn Penaeus monodon [50]. …”

Comparative phylogeography of three host sea anemones in the Indo‐Pacific

“…We found that there is a significant congruence of patterns of genetic differentiation among species and that the Maldives (western/central Indian Ocean) represents a location of overlap or possible hybridization among distinct anemone populations or lineages (Sheppard et al, ). Previous studies have reported genetic discontinuity between the eastern and western Indian Ocean in different taxa including coral reef fishes (Bay, Choat, van Herwerden, & Robertson, ; Gaither et al, ; Huyghe & Kochzius, ; Leray et al, ) and invertebrates such as echinoderms (Otwoma & Kochzius, ; Vogler et al, ) and giant clams (Hui et al, ). Only one of these included samples from the Maldives (Vogler et al, ) and did not report overlap of different clades at these islands.…”

“…Many marine species are endemic to the Indo‐Pacific region and some of these have evolved symbiotic relationships, such as the iconic association between host sea anemones (Order Actiniaria) and anemonefishes (Genera Amphiprion and Premnas ; Fautin & Allen, ; Allen, Drew, & Fenner, ). A number of studies report large‐scale population genetic structure of anemonefishes (Dohna, Timm, Hamid, & Kochzius, ; Huyghe & Kochzius, ; Nanninga et al, ; O'Donnell, Beldade, Mills, Williams, & Bernardi, ; Saenz‐Agudelo et al, ; Steinberg et al, ; Timm & Kochzius, ). In general these studies indicate that anemonefish species such as Amphiprion bicinctus , Amphiprion ocellaris and Amphiprion perideraion display genetic structure that coincides with historical geographical barriers such as the Sunda shelf, the Straight of Bab Al Mandeb, between basins (Pacific Ocean and Indian Ocean) or between the eastern and western sides of the Indian Ocean.…”

“…Many marine species are endemic to the Indo-Pacific region and some of these have evolved symbiotic relationships, such as the iconic association between host sea anemones (Order Actiniaria) and anemonefishes (Genera Amphiprion and Premnas; Fautin & Allen, 1997;Allen, Drew, & Fenner, 2010). A number of studies report largescale population genetic structure of anemonefishes (Dohna, Timm, Hamid, & Kochzius, 2015;Huyghe & Kochzius, 2017;Nanninga et al, 2014;O'Donnell, Beldade, Mills, Williams, & Bernardi, 2017;Saenz-Agudelo et al, 2015;Steinberg et al, 2016;Timm & Kochzius, 2008).…”