Temporal evolution of coral reef fishes: global patterns and disparity in isolated locations

Abstract

Aim Many coral reef regions have a history of isolation and extinction. Our aim was to test whether the disparate evolutionary and biogeographical histories of the world's coral reef regions have significantly impacted temporal patterns of speciation within regions. In essence, do assemblages in peripheral locations contain the youngest coral reef fish species? Location Pan‐tropical coral reef systems. Methods Molecular data (mitochondrial 16S rRNA, 12S rRNA, CO1, cytochrome b; nuclear TMO‐4C4, S7 intron 1) were assembled for genera with near‐complete taxon sampling (minimum 70% nominal species) from four major coral reef fish families (Chaetodontidae, Labridae, Pomacanthidae and Serranidae). This was combined with fossil data to simultaneously infer the phylogeny and estimate species' divergence times. species' distributions were quantified using IUCN maps and the ages of species with different biogeographical extents were compared. Model fitting was used to compare the distribution of species' ages across the whole phylogeny with age distributions of species restricted to the Red Sea and Hawaiian Islands. Results Temporal patterns of coral reef fish divergence were similar among major marine realms and regions. However, notable differences were recorded between the Red Sea and Hawaiian Islands. Red Sea endemics have diverged consistently throughout the last 16 Myr, whereas endemic species colonized the Hawaiian Islands in two distinct waves (0–3 Ma and 8–12 Ma). Differences in the proportions of allopatric and sympatric sister‐species between Red Sea and Hawaiian endemics were also detected. Main conclusions Despite differing geological histories, marine realms and regions have all experienced comparable and relatively recent divergences of extant coral reef fish species. Differences in age distributions and spatial relationships of endemic species in the Red Sea and Hawaiian Islands suggest that markedly different processes have shaped patterns of diversification in these peripherally isolated locations.

The evolution of fishes and corals on reefs: form, function and interdependence

“…The mean (crown) ages (white bars; ±S.E.) of fish families (F) and genera (G) were calculated based on the ages taken from published time-calibrated phylogenies (Cowman & Bellwood, 2011: Chaetodontidae, Labridae, Pomacentridae;Sorenson et al, 2013: Acanthuridae) with mean ages of fish species (Sp) from Hodge et al (2014). Taxon ages for corals were calculated based on the time-calibrated phylogeny of Huang & Roy (2013).…”

“…Although there is considerable variation in rates of diversification among the major ocean basins (Cowman & Bellwood, 2013b;Bellwood et al, 2015b), the mean ages of reef fish species among regions (or more accurately the estimated divergence times of species; Hodge & Bellwood, 2015) are remarkably consistent at about 5.3 Myr. If only sister species are considered (excluding species which have sister lineages that have subsequently diverged) the mean age of separation is about 2.9 Myr (Hodge et al, 2014;Hodge & Bellwood, 2015). Corals likewise show relatively recent diversification, although the mean age of 1.9 Myr is likely to change as more families are considered and trees are better resolved.…”

“…Early work suggested that colour-based sexual dimorphism was key to species-level diversification in parrotfishes, following an earlier stage of ecomorphological differentiation (Streelman et al, 2002). Yet recent species-level phylogenies suggest that speciation in parrotfishes is primarily related to geographic barriers, mostly within the last 4 Myr (Choat et al, 2012;Hodge et al, 2014;Hodge & Bellwood, 2015). Thus colour may help stabilize population divisions and facilitate subsequent diversification (it also provides a widely used basis for taxonomic divisions), but it does not appear to have driven speciation in this group.…”

“…Alfaro et al, 2009;Cowman & Bellwood, 2011), and the biogeographic factors shaping patterns and modes of speciation (e.g. Hodge et al, 2012;Bowen et al, 2013;Hodge, van Herwerden & Bellwood, 2014). These advances were driven largely by analyses of molecular phylogenies, complemented by new evidence from the fossil record.…”

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

“…The Indo-Pacific Barrier (i.e. Sunda Shelf) is ephemeral however, with separate Indian and Pacific Ocean faunas at glacial maxima, followed by a biogeographic gradient during interglacial periods as the two faunas expand into the alternate ocean basin (Briggs and Bowen, 2012;Gaither and Rocha, 2013;Hodge et al, 2014;Eble et al, 2015). Hence, evolutionary divergence between sister taxa may begin at the glacial-induced barrier, but species cohesion depends on maintaining separate gene pools during the interglacial periods of secondary contact (Chenoweth et al, 1998;van Herwerden and Doherty, 2006;Sorenson et al, 2014 (Fig 2c).…”