Seascape genetics along environmental gradients in the Arabian Peninsula: insights from ddRAD sequencing of anemonefishes

Abstract

Understanding the processes that shape patterns of genetic structure across space is a central aim of landscape genetics. However, it remains unclear how geographical features and environmental variables shape gene flow, particularly for marine species in large complex seascapes. Here, we evaluated the genomic composition of the two-band anemonefish Amphiprion bicinctus across its entire geographical range in the Red Sea and Gulf of Aden, as well as its close relative, Amphiprion omanensis endemic to the southern coast of Oman. Both the Red Sea and the Arabian Sea are complex and environmentally heterogeneous marine systems that provide an ideal scenario to address these questions. Our findings confirm the presence of two genetic clusters previously reported for A. bicinctus in the Red Sea. Genetic structure analyses suggest a complex seascape configuration, with evidence of both isolation by distance (IBD) and isolation by environment (IBE). In addition to IBD and IBE, genetic structure among sites was best explained when two barriers to gene flow were also accounted for. One of these coincides with a strong oligotrophic-eutrophic gradient at around 16-20˚N in the Red Sea. The other agrees with a historical bathymetric barrier at the straight of Bab al Mandab. Finally, these data support the presence of interspecific hybrids at an intermediate suture zone at Socotra and indicate complex patterns of genomic admixture in the Gulf of Aden with evidence of introgression between species. Our findings highlight the power of recent genomic approaches to resolve subtle patterns of gene flow in marine seascapes.

Consequences of marine barriers for genetic diversity of the coral‐specialist yellowbar angelfish from the Northwestern Indian Ocean

“…The presence of a genetic discontinuity between both sides of the Arabian Peninsula as shown here for P. maculosus, coincides with previous population genetic reports from both mitochondrial DNA of Cephalopholis hemistiktos (Priest et al, 2016) and from double digest RAD sequencing (ddRAD-seq) of Amphiprion bicinctus and A. omanesis (Saenz-Agudelo et al, 2015), which in turn also presented a genetic break within the Red Sea (Nanninga et al, 2014). The presence of a genetic discontinuity between both sides of the Arabian Peninsula as shown here for P. maculosus, coincides with previous population genetic reports from both mitochondrial DNA of Cephalopholis hemistiktos (Priest et al, 2016) and from double digest RAD sequencing (ddRAD-seq) of Amphiprion bicinctus and A. omanesis (Saenz-Agudelo et al, 2015), which in turn also presented a genetic break within the Red Sea (Nanninga et al, 2014).…”

Genomic analysis of a cardinalfish with larval homing potential reveals genetic admixture in the Okinawa Islands

“…Overall our study supports the importance of examining the degree of genetic differentiation within various geographic regions for a range of fish species as well as species‐specific patterns across groups of reef fishes to better understand the relationships between life‐history traits, larval behaviour and gene flow. We highlight the effectiveness of RAD‐Seq methods, which have recently been applied to examine the genomics of other coral reef fishes (Gaither et al., ; Picq, McMillan, & Puebla, ; Puebla, Bermingham, & McMillan, ; Saenz‐Agudelo et al., ; Stockwell et al., ), to study such nonmodel organisms. Our results show that in contrast to other cardinalfish species (Bernardi & Vagelli, ; Gerlach et al., ; Gotoh et al., ; Hoffman et al., ; Vagelli et al., ), S. tubifer exhibits genetic admixture over a 140‐km region despite the species’ demonstrated homing abilities and olfactory preferences for a home reef (Gould et al., ).…”

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

“…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.…”