Patterns of species range evolution in Indo-Pacific reef assemblages reveal the Coral Triangle as a net source of transoceanic diversity

Abstract

The Coral Triangle in the Indo-Pacific is a region renowned for exceptional marine biodiversity. The area could have acted as a ‘centre of origin’ where speciation has been prolific or a ‘centre of survival’ by providing refuge during major environmental shifts such as sea-level changes. The region could also have acted as a ‘centre of accumulation’ for species with origins outside of the Coral Triangle, owing to it being at a central position between the Indian and Pacific oceans. Here, we investigated support for these hypotheses using population-level DNA sequence-based reconstructions of the range evolution of 45 species (314 populations) of Indo-Pacific reef-associated organisms. Our results show that populations undergoing the most ancient establishment were significantly more likely to be closer to the centre of the Coral Triangle than to peripheral locations. The data are consistent with the Coral Triangle being a net source of coral-reef biodiversity for the Indo-Pacific region, suggesting that the region has acted primarily as a centre of survival, a centre of origin or both. These results provide evidence of how a key location can influence the large-scale distributions of biodiversity over evolutionary timescales.

The origin and evolution of coral species richness in a marine biodiversity hotspot*

“…Although large-scale dispersal of reef corals in the Indo-Pacific remains poorly understood, recent studies have suggested that dispersal out of the CT may increase during episodes of global warming (Burrows et al 2011;Kiessling et al 2012), and the CT may be a net larval source under current environmental conditions (Wood et al 2014). A population-level analysis of 45 Indo-Pacific reef-associated species also found that population establishments closer to the CT were generally older than those at peripheral locations, indicating that the CT has been a net source of biodiversity for the Indo-Pacific region (Evans et al 2016). In reconciling these more recent patterns with our results, it is important to note the difference in temporal and taxonomic scales involved and also that range expansions such as those documented here necessarily involve not only arrival, but also establishment and persistence of populations in a new locality.…”

“…A population‐level analysis of 45 Indo‐Pacific reef‐associated species also found that population establishments closer to the CT were generally older than those at peripheral locations, indicating that the CT has been a net source of biodiversity for the Indo‐Pacific region (Evans et al. ). In reconciling these more recent patterns with our results, it is important to note the difference in temporal and taxonomic scales involved and also that range expansions such as those documented here necessarily involve not only arrival, but also establishment and persistence of populations in a new locality.…”

“…With the exception of some earlier studies of reef corals (e.g., Stehli and Wells ; Pandolfi ), exploration of the macroevolutionary dynamics underlying the CT species richness peak has been dominated by data from reef fish along with some isolated studies of invertebrates (reviewed in Cowman ; Barber and Meyer ; Evans et al. ). Given the ecological and conservation importance of reef‐building corals, there is clearly a need to better understand the macroevolutionary underpinnings of the high coral species richness in the CT.…”

Genomic signatures of host‐associated divergence and adaptation in a coral‐eating snail, Coralliophila violacea (Kiener, 1836)

“…While there is ongoing debate (Evans, McKenna, Simpson, Tournois, & Genner, 2016;Huang, Goldberg, Chou, & Roy, 2018;Di Martino, Jackson, Taylor, & Johnson, 2018;Matias & Riginos, 2018), there is clearly a multiplicity of processes driving diversification in this region (Barber & Meyer, 2015). Given the results of this study, it is important to expand our thinking beyond models that focus solely on allopatry to advance our understanding of marine speciation and origins of the Coral Triangle biodiversity hotspot.…”

Evolutionary ecology of species ranges in aquatic environments

“…Here, reef species diversity is positively associated with persistence of reef habitat during sea-level changes over the last 3 million years [8]. This concept of the Coral Triangle acting as source of contemporary species diversity across the Indo-Pacific was further investigated by Evans et al [9], who used molecular data to estimate the relative ages of populations in each of 46 reef-associated species. Focal species were more likely to have older populations closer to the Coral Tringle, consistent with the region being a centre of survival from which they have dispersed and colonized the wider region.…”