Flickers of speciation: Sympatric colour morphs of the arc‐eye hawkfish,Paracirrhites arcatus, reveal key elements of divergence with gene flow

Abstract

One of the primary challenges of evolutionary research is to identify ecological factors that favour reproductive isolation. Therefore, studying partially isolated taxa has the potential to provide novel insight into the mechanisms of evolutionary divergence. Our study utilizes an adaptive colour polymorphism in the arc-eye hawkfish (Paracirrhites arcatus) to explore the evolution of reproductive barriers in the absence of geographic isolation. Dark and light morphs are ecologically partitioned into basaltic and coral microhabitats a few metres apart. To test whether ecological barriers have reduced gene flow among dark and light phenotypes, we evaluated genetic variation at 30 microsatellite loci and a nuclear exon (Mc1r) associated with melanistic coloration. We report low, but significant microsatellite differentiation among colour morphs and stronger divergence in the coding region of Mc1r indicating signatures of selection. Critically, we observed greater genetic divergence between colour morphs on the same reefs than that between the same morphs in different geographic locations. We hypothesize that adaptation to the contrasting microhabitats is overriding gene flow and is responsible for the partial reproductive isolation observed between sympatric colour morphs. Combined with complementary studies of hawkfish ecology and behaviour, these genetic results indicate an ecological barrier to gene flow initiated by habitat selection and enhanced by assortative mating. Hence, the arc-eye hawkfish fulfil theoretical expectations for the earliest phase of speciation with gene flow.

Multilocus molecular systematics of the circumtropical reef-fish genus Abudefduf (Pomacentridae): history, geography and ecology of speciation

“…Color is of paramount importance for hamlets as the vast majority of matings are between individuals of the same color ( Barreto & McCartney, 2008 ; Fischer, 1980 ; Puebla et al, 2007 ), and both natural and sexual selection can act to generate assortative mating that will in turn lead to reproductive isolation and speciation even with gene flow ( Puebla, Bermingham & Guichard, 2012 ). Presence of color-assortative mating in Chaetodontidae ( McMillan, Weigt & Palumbi, 1999 ), Serranidae (see references above) and Cirrhitidae ( Whitney, Bowen & Karl, 2018 ) indicates that the process is generally distributed among reef fishes. Hence, the idea that within planktivorous Abudefduf , an ability to vary color may have promoted assortative color-based mating that facilitate speciation and the creation of regional endemics is not unreasonable.…”

Does color matter? Molecular and ecological divergence in four sympatric color morphs of a coral reef fish

“…In allopatry, divergent color morphology is often accompanied by genetic partitions (Drew et al., 2008, 2010; Taylor & Hellberg, 2003). However, published studies on divergent non‐sex‐linked color morphs in sympatry are rare (Whitney, Bowen, et al, 2018; Whitney, Donahue, et al, 2018). Paracirrhites forsteri displays sympatric color morphs that vary in appearance and abundance throughout the Indo‐West Pacific.…”

“…Stable and sympatric color morphs have been documented in three of the six species in the genus Paracirrhites ( P. forsteri , P. arcatus , and P. hemistictus ) (Randall, 2005; Whitney, Donahue, & Karl, 2018). The two non‐sex‐linked color morphs of P. arcatus show a strong correlation between phenotype and environment on Hawaiian reefs (Whitney, Donahue, et al, 2018), as well as significant divergence at microsatellite loci and a gene associated with coloration (Whitney, Bowen, et al, 2018). Taken together, these data support the possibility of at least partial assortative mating among the two color morphs of P. arcatus .…”

The combined use of raw and phylogenetically independent methods of outlier detection uncovers genome‐wide dynamics of local adaptation in a lizard

“…In addition, admixture may also have been important for maintaining populations adapted to changing local conditions. Thus, a variable permeability to immigration conditioned by a dynamic landscape configuration may have prevented speciation while maintaining strong genetic structure (Räsänen & Hendry, 2008;Whitney, Bowen, & Karl, 2018). This is remarkable for a terrestrial vertebrate with limited dispersal ability (Santos et al, 2008) after 3 millions of years of lineage divergence (Carranza et al, 2006).…”