Global physical controls on estuarine habitat distribution during sea level change: Consequences for genetic diversification through time

Determining the extrinsic (physical) factors controlling speciation and diversification of species through time is of key interest in paleontology and evolutionary biology. The role of sea-level change in shaping species richness patterns of marginal marine species has received much attention, but with variable conclusions. Recent work combining genetic data and Geographical Information Systems (GIS)-based habitat modeling yielded a framework for how geomorphology of continental margins mediates genetic connectivity of populations during sea-level change. This approach may ultimately yield insights on how distinct lineages, species, and biodiversity accumulate in coastal settings. Here, we expand this GIS work globally to different geomorphic settings to model estuarine habitat in a larger geographic framework and test how tectonic setting, oceanographic setting, climate, and margin age affect habitat distribution during sea-level change. In addition, independent of estuaries we explore paleobiologic (e.g. Olsson, 1961) and neontolologic effects of sea-level change on evolution, and test the relation between overall shelf area and species richness using data of 1721 fish species. We find 82% global reduction of estuarine habitat abundance at lowstand relative to highstand, and find large habitats change in size much more than small habitats. Consistent with prior work, narrow continental margins have significantly less habitat at highstand and lowstand than wide margins, and narrow margins significantly associate with fore-arc settings, effectively linking tectonic setting to habitat abundance. Surprisingly, narrow margins host greater species richness, a finding which violates the canonical species-area relation. This finding can be explained if: 1) the physical isolation imposed by narrow margins facilitates the formation of new species over time; 2) the size-stability of small habitats, which disproportionately occur on narrow margins, accumulate and retain species extirpated in the more variable habitats on wide margins; or 3) the smaller habitats on narrow margins facilitate greater species richness through greater habitat heterogeneity. These results are generally at odds with prior interpretations, but the combination of richness data and population genetic principles offer a different perspective on these long-studied questions. Finally, we emphasize that the nuance of Pleistocene-Holocene sea level oscillations should be more explicitly considered in genetic studies.