Evolutionary Dynamics in the Southwest Indian Ocean Marine Biodiversity Hotspot: A Perspective from the Rocky Shore Gastropod Genus Nerita

Abstract

The Southwest Indian Ocean (SWIO) is a striking marine biodiversity hotspot. Coral reefs in this region host a high proportion of endemics compared to total species richness and they are particularly threatened by human activities. The island archipelagos with their diverse marine habitats constitute a natural laboratory for studying diversification processes. Rocky shores in the SWIO region have remained understudied. This habitat presents a high diversity of molluscs, in particular gastropods. To explore the role of climatic and geological factors in lineage diversification within the genus Nerita, we constructed a new phylogeny with an associated chronogram from two mitochondrial genes [cytochrome oxidase sub-unit 1 and 16S rRNA], combining previously published and new data from eight species sampled throughout the region. All species from the SWIO originated less than 20 Ma ago, their closest extant relatives living in the Indo-Australian Archipelago (IAA). Furthermore, the SWIO clades within species with Indo-Pacific distribution ranges are quite recent, less than 5 Ma. These results suggest that the regional diversification of Nerita is closely linked to tectonic events in the SWIO region. The Reunion mantle plume head reached Earth’s surface 67 Ma and has been stable and active since then, generating island archipelagos, some of which are partly below sea level today. Since the Miocene, sea-level fluctuations have intermittently created new rocky shore habitats. These represent ephemeral stepping-stones, which have likely facilitated repeated colonization by intertidal gastropods, like Nerita populations from the IAA, leading to allopatric speciation. This highlights the importance of taking into account past climatic and geological factors when studying diversification of highly dispersive tropical marine species. It also underlines the unique history of the marine biodiversity of the SWIO region.

Patterns and drivers of species diversity in the Indo‐Pacific red seaweed Portieria

“…From there, species dispersed north‐ and southward, and speciated along a temperature gradient or across temperature barriers in the Somali‐Arabian region and temperate southern Africa, respectively. This supports the Southwestern and Northwestern Indian Oceans as generators of biodiversity, as has been indicated for several marine animal groups, including brittle‐stars (Hoareau, Boissin, Paulay, & Bruggemann, ) and gastropods (Postaire, Bruggemann, Magalon, & Faure, ). Upwelling systems in the Northwestern Indian Ocean have been shown to create stark biogeographical delineations in marine species composition (Burt et al., ; Schils & Wilson, ) and are a likely driver of speciation.…”

“…This supports the Southwestern and Northwestern Indian Oceans as generators of biodiversity, as has been indicated for several marine animal groups, including brittle-stars (Hoareau, Boissin, Paulay, & Bruggemann, 2013) and gastropods (Postaire, Bruggemann, Magalon, & Faure, 2014). Upwelling systems in the Northwestern Indian…”

Fish community structure in relation to environmental variation in coastal volcanic habitats

“…This theoretical approach was essential in order to assess the distribution of rare species and especially species not previously recorded from Reunion Island. This method, however, ignores the evolutionary constraints, providing ranges that would be possible if dispersal was not limited by geological history, which is particularly complex in volcanic oceanic islands (Postaire et al, 2014). It is therefore possible that some model-based distribution patterns are broader than what exist in reality.…”

“…If long distance settlement events seem to be the most frequent speciation mechanism of marine species with the modification of gene flow through time due to changes in biotic and abiotic conditions (Paulay, 2006), other processes like disruptive selection, habitat or resource choice, may occur at smaller geographic scales and lead to sympatric sister-species (Postaire et al, 2014). Moreover, the global cooling that occurred during Oligo-Miocene (23 Ma) caused transient lowerings in sea levels that expanded emerged landmasses and coastlines (Haq et al, 1987).…”

“…Otherwise, the southwestern Indian Ocean (SWIO) region, comprising a main landmass, Madagascar, and several island archipelagos such as Comoros, Mascarenes and Seychelles, each with different origins and ages, hosts a high proportion of endemics and is highly threatened by human activities, hence its classification as a marine biodiversity hotspot (Bellard et al, 2013;Roberts et al, 2002). This region constitutes a natural laboratory for studying diversification processes in coastal marine taxa, whose rocky shore species have been yet little studied (Postaire et al, 2014).…”