Hierarchical behaviour, habitat use and species size differences shape evolutionary outcomes of hybridization in a coral reef fish

Abstract

Keywords:Amphiprion leucokranos; asymmetric behavioural isolation; reproductive barrier; size-based hierarchy; unidirectional introgression. AbstractHybridization is an important evolutionary process, with ecological and behavioural factors influencing gene exchange between hybrids and parent species. Patterns of hybridization in anemonefishes may result from living in highly specialized habitats and breeding status regulated by size-based hierarchal social groups. Here, morphological, ecological and genetic analyses in Kimbe Bay, Papua New Guinea, examine the hybrid status of Amphiprion leucokranos, a nominal species and presumed hybrid between Amphiprion sandaracinos and Amphiprion chrysopterus. We test the hypothesis that habitat use and relative size differences of the parent species and hybrids determine the patterns of gene exchange. There is strong evidence that A. leucokranos is a hybrid of smaller A. sandaracinos and larger A. chrysopterus, where A. chrysopterus is exclusively the mother to each hybrid, based on mtDNA cytochrome b and multiple nDNA microsatellite loci. Overlap in habitat, depth and host anemone use was found, with hybrids intermediate to parents and cohabitation in over 25% of anemones sampled. Hybrids, intermediate in body size, colour and pattern, were classified 55% of the time as morphologically first-generation hybrids relative to parents, whereas 45% of hybrids were more A. sandaracinos-like, suggesting backcrossing. Unidirectional introgression of A. chrysopterus mtDNA into A. sandaracinos via hybrid backcrosses was found, with larger female hybrids and small male A. sandaracinos mating. Potential nDNA introgression was also evident through distinct intermediate hybrid genotypes penetrating both parent species. Findings support the hypothesis that anemonefish hierarchical behaviour, habitat use and species-specific size differences determine how hybrids form and the evolutionary consequences of hybridization.

Phylogeography of the sergeantsAbudefduf sexfasciatusandA. vaigiensisreveals complex introgression patterns between two widespread and sympatric Indo‐West Pacific reef fishes

“…However, this hypothesis is unlikely in damselfishes which lay demersal eggs (Gainsford et al . ) as do A. sexfasciatus and A. vaigiensis . Relative differences in population density may also favour hybridization.…”

“…Two species that form heterospecific social groups and have synchronized spawning seasons may experience external fertilization accidentally involving gametes of both species. However, this hypothesis is unlikely in damselfishes which lay demersal eggs (Gainsford et al 2015) as do A. sexfasciatus and A. vaigiensis. Relative differences in population density may also favour hybridization.…”

Introgression and selection shaped the evolutionary history of sympatric sister‐species of coral reef fishes (genus: Haemulon)

“…; Gaither et al . ). Overall, this study represents a substantial increase in the number of specimens and genomic resources available for H. maculicauda and H. flaviguttatum .…”

“…However, recent studies have found evidence of hybridization and introgression in several marine fishes (Arnold & Fogarty 2009;Richards & Hobbs 2015). In coral reef fishes, examples include butterflyfishes (Pyle & Randall 1994;Montanari et al 2012), anemonefishes (Litsios & Salamin 2014;Gainsford et al 2015), grunts (Rocha et al 2008;Bernardi et al 2013), hamlets (Puebla et al 2007(Puebla et al , 2014, angelfishes (Schultz et al 2006;Gaither et al 2014), surgeonfishes (DiBattista et al 2011, wrasses (Pyle & Randall 1994;Yaakub et al 2007), groupers (Harrison et al 2014;Payet et al 2016) and damselfishes (Coleman et al 2014). Further, hotspots of hybridization have been found in the boundaries of marine biogeographic provinces.…”

Widespread hybridization and bidirectional introgression in sympatric species of coral reef fish

“…Naturally occurring hybrids among coral reef fishes were once thought to be rare (Hubbs, 1955), although recent studies have identified over 75 species of coral reef fish that hybridize in the wild (Montanari, Hobbs, Pratchett, & van Herwerden, 2016;Yaakub, Bellwood, Herwerden, & Walsh, 2006) and many more cases of natural hybridization continue to be described (e.g., DiBattista et al, 2016;Gainsford, Van Herwerden, & Jones, 2015;Hobbs, Frisch, Allen, & van Herwerden, 2009;Marie, Van Herwerden, Choat, & Hobbs, 2007;Montanari, van Herwerden, Pratchett, Hobbs, & Fugedi, 2012;Payet et al, 2016). Most of these studies have been conducted in well-known suture zones, where biogeographic regions collide and numerical disparity between parent species can result in accidental hybridization (DiBattista et al, 2015;Richards & Hobbs, 2015).…”