When biogeographical provinces collide: hybridization of reef fishes at the crossroads of marine biogeographical provinces in the Arabian Sea

Abstract

Aim Suture zones are areas where closely related species from different biogeographical regions come into contact and interbreed. This concept originated from the study of terrestrial ecosystems but it remains unclear whether a similar phenomenon occurs in the marine environment. Here we investigate a potential suture zone from a previously unknown hybrid hotspot at the Socotra Archipelago (Yemen), located in the Arabian Sea, where fauna from the Red Sea, Gulf of Aden, Arabian Sea, western Indian Ocean and greater Indo‐Polynesian Province intersect. Location Red Sea, Gulf of Aden, Arabian Sea and Indian Ocean. Methods Putative hybrid reef fish were identified based on intermediate coloration and morphology. Underwater observations and collections were conducted to determine: (1) whether parent species form heterospecific social groups or breeding pairs; (2) the sex and reproductive status of morphologically intermediate individuals; and (3) whether parent species were forming mixed species associations owing to a dearth of conspecific partners. To support hybrid status, morphologically intermediate and parental individuals were genotyped using mitochondrial DNA cytochrome c oxidase subunit I (COI), nuclear recombination‐activating gene 2 (RAG2) and the nuclear TMO‐4C4 (TMO) gene. Results We observed putative hybrids involving 14 species from four reef fish families at Socotra. Most cases involved a parental species with a restricted distribution (e.g. Red Sea or Arabian Sea) and a broadly distributed Indo‐Pacific species. In most cases, at least one of the parent species was rare at Socotra. Hybrid gene flow was largely unidirectional, and although introgression was rare, we found evidence that some butterflyfish and surgeonfish hybrids were fertile and formed breeding groups with parental species. Main conclusions The rate of hybrid discovery at Socotra is much greater than that recorded elsewhere in the marine environment and involved both allopatric and sympatric species. This study highlights the importance of biogeographical location, reef habitat, environmental conditions and abundance disparities at Socotra in potentially facilitating hybridization among reef fishes at the edge of their distribution.

Surgeons and suture zones: Hybridization among four surgeonfish species in the Indo-Pacific with variable evolutionary outcomes

“…It is now evident that hybridization in reef fishes occurs under different scenarios, and across a range of taxa and geographic locations Hobbs and Allen, 2014;DiBattista et al, 2015). Hybridization in reef fishes has a range of evolutionary consequences (Richards and Hobbs, 2014), even within a species complex (this study).…”

“…All of these processes may occur in young hybridizing species and overlap to produce similar genetic signatures. The presence of suture zones allows for comparative studies across multiple taxa that are hybridizing in one location (Hobbs and Allen, 2014;DiBattista et al, 2015). Furthermore, species complexes (such as the A. nigricans complex) that span multiple suture zones provide an ideal scenario to determine the role that hybridization plays in the evolutionary history of reef fishes.…”

“…Hobbs and Allen, 2014;DiBattista et al, 2015) and includes surgeonfishes (Randall, 2002;Marie et al, 2007), butterflyfishes (McMillan et al, 1999;, angelfishes (Pyle and Randall, 1994), wrasses (Yaakub et al, 2006(Yaakub et al, , 2007, damselfishes (van Herwerden and Doherty, 2006) and groupers . Although morphological characterization of hybrids is still common, molecular techniques can reveal hybrids that may otherwise go undetected (Kuriiwa et al, 2007;Montanari et al, 2012Montanari et al, , 2014 and the geographic extent of introgression (McMillan et al, 1999).…”

“…Climatic cycles over the past 2 million years have allowed allopatric divergence of Indian and Pacific lineages, which have since come back into contact in this area (Briggs and Bowen, 2012). Another prominent suture zone for reef fishes was recently discovered in the Socotra Archipelago, at the intersection of four biogeographic provinces in the north-western Indian Ocean (DiBattista et al, 2015). More suture zones are suspected in southern Japan and the Marshall Islands .…”

Species delimitation in the coral genus Goniopora (Scleractinia, Poritidae) from the Saudi Arabian Red Sea

“…Although widespread in the Indo-Pacific (Veron, 2000), the genus remained understudied except for two recent works by Kitano et al (2013Kitano et al ( , 2014 that investigated the phylogenetic relationships of several species with a particular focus on specimens from Japan. This is the first work using molecular approaches to the biodiversity of the genus within an underexplored and species-rich region such as the Red Sea, where a wide range of marine organisms are increasingly being investigated using combined morpho-molecular data (e.g., HaverkortYeh et al, 2013;DiBattista et al, 2013DiBattista et al, , 2015Terraneo et al, 2014;Huang et al, 2014;Arrigoni et al, 2015;van der Meij et al, 2015;Spaet and Berumen, 2015).…”