INFERRING SPECIATION AND POST-SPECIATION DIVERGENCE BY DEPTH PARAPATRY

Inferring modes of speciation is foundational to evolutionary biology. Identifying the mechanisms that drive post-speciation divergence in the sea is particularly challenging. Speciation by depth parapatry, caused by divergent adaptations of an ancestral species to multiple ecological niches up and down the water column, has long been considered a viable mode of speciation to explain the co-occurrence of multiple forms at a single site despite incomplete barriers to gene flow and without invoking secondary contact. Tracking the movement of new species into new ecological niches does however necessitate a fossil record with outstanding resolution in morphological, stratigraphic, geochemical, and taxonomic dimensions.

Here, we analyse geochemical traits before, during and after speciation in the Menardella limbata – Menardella exilis – Menardella pertenuis lineage of macroperforate planktonic foraminifera from the Plio-Pleistocene western equatorial Atlantic Ocean. Deploying improved protocols for laser ablation inductively coupled plasma mass spectrometry to quantify the elemental composition of the foraminiferal calcium carbonate shell, we analyse >7000 laser shots in ~1000 foraminifers at multiple growth stages per individual.

Inferred thermal niche occupation overlaps for all species in their terminal stage, but there is a clear ontogenetic shift through speciation: ancestral species demonstrate a marked increase in Mg/Ca ratios during life, whereas descendent species show no detectable changes. Zooming into the split from ancestor to descendant reveals how the ontogenetic shift steepens during the establishment of Menardella exilis. The strengthening bifurcation through the speciation interval suggests that isolation-by-depth can occur rapidly as a facilitator of divergence despite incomplete barriers to gene flow, helping explain the ongoing conundrum of speciation in the sea.