4.4 Sea surface temperature as a major diversification driver in marine organisms?
Conversely to pelagic fishes that show no or low inter-ocean structure (Díaz-Jaimes et al. 2010, Ely et al. 2005) and no intra-ocean structure (Nomura et al. 2014, Taguchi et al. 2015), sea mammal’s gene flow is shaped by sea temperature which drives structuration between ocean basins and among breeding areas (Alexander et al. 2016, Jackson et al. 2014, Richard et al. 2018, Fontaine et al. 2014, Viricel & Rosel 2014). SST plays also a role in the diversification of sea turtles, since only cold-adapted species are able to exchange genes among oceans (Dutton et al. 1999). Finally, organisms with a pelagic larval phase show globally low structuration (Kelly & Palumbi 2010) but when detected, structuration is often linked to sea temperature (Benestan et al. 2015; Teske et al. 2005, 2018). Therefore, SST appears as a generic driver of diversification in marine organisms, though their patterns of structuration are generally considerably weaker (see Bowen et al. 2016 for a review) than those found here. We suggest that the reason for this discrepancy lies in the fact that these seabirds are central place foragers, i.e. they still depend on terrestrial habitats for breeding, the latter being impacted for instance by glaciations. They are therefore highly sensitive to any latitudinal change of SST in comparison to island distribution, which acts as a constraint since an optimal area in regard to SST may lack any island for breeding. Indeed, in marine organisms with low dispersal abilities, patterns of structuration and divergence are more similar to the patterns found here on shearwaters. For instance, timing of population divergence between Atlantic and Indian Ocean lineages and within the Atlantic in the seahorse Hippocampus ’kuda complex’ (Floeter et al. 2007) fits to our estimates. This species has no planktonic larval duration (Lourie et al. 2005) and long dispersal events are considered rare and implying a few individuals (Teske et al. 2005). Moreover, Cape Agulhas is known to be a phylogeographic break among several costal species, due to the difference of currents and sea temperatures between the two oceans (review in Teske et al. 2011). On the other extreme, seabirds do not compare either to terrestrial organisms living on islands, despite being highly philopatric, simply because they can disperse easily, if an island is available to being colonised.
In this small shearwater complex, geographical barriers and/or isolation by distance may have been a major driver of differentiation at large scale (typically, between Oceans) while SST has been a more important driver at smaller scale (within Oceans), with shearwaters shifting their breeding latitudes with a changing SST. However, since these seabirds depend on the geographical distribution of their breeding islands and because these seabirds are not the best seabird fliers, this distribution becomes a major constraint resulting in the present geographical structure, promoting local adaptation to small scale ecological constraints and reducing gene flow. Therefore, petrels and shearwaters present an interesting case study where diversification processes rely more (or at least equally) on ecological factors, in particular sea surface temperature, rather than distance or continental barriers, in contrast to either “true” marine organisms or terrestrial organisms. Strict marine organisms can disperse far more, or alternatively are unconstrained by island distribution, and thus show much less geographical structure within taxa. The terrestrial organisms tend to disperse far less, and isolation-by-distance tends to be a main driver of population differentiation (Meirmans 2012; Vekemans & Hardy 2004). Indeed terrestrial organisms, such as lizards or birds in Macaronesia (AlmalkI et al. 2017; Brehm et al. 2003), geckos in Cape Verde (Arnold et al. 2008) or birds in America (Patel et al. 2011), have revealed strong splits between islands with no shared haplotypes for the same mitochondrial markers.