Long prereproductive selection and divergence by depth in a Caribbean candelabrum coral

Abstract

Long-lived corals, the foundation of modern reefs, often follow ecological gradients, so that populations or sister species segregate by habitat. Adaptive divergence maintains sympatric congeners after secondary contact or may even generate species by natural selection in the face of gene flow. Such ecological divergence, initially between alternative phenotypes within populations, may be aided by immigrant inviability, especially when a long period separates larval dispersal and the onset of reproduction, during which selection can sort lineages to match different habitats. Here, we evaluate the strength of one ecological factor (depth) to isolate populations by comparing the genes and morphologies of pairs of depth-segregated populations of the candelabrum coral Eunicea flexuosa across the Caribbean. Eunicea is endemic to the Caribbean and all sister species co-occur. Eunicea flexuosa is widespread both geographically and across reef habitats. Our genetic analysis revealed two depth-segregated lineages. Field survivorship data, combined with estimates of selection coefficients based on transplant experiments, suggest that selection is strong enough to segregate these two lineages. Genetic exchange between the Shallow and Deep lineages occurred either immediately after divergence or the two have diverged with gene flow. Migration occurs asymmetrically from the Shallow to Deep lineage. Limited recruitment to reproductive age, even under weak annual selection advantage, is sufficient to generate habitat segregation because of the cumulative prolonged prereproductive selection. Ecological factors associated with depth can act as filters generating strong barriers to gene flow, altering morphologies, and contributing to the potential for speciation in the sea.

Testing the depth-differentiation hypothesis in a deepwater octocoral

“…This could lead to selection, and thus adaptive divergence among populations occupying different depths [60]. Pre-reproductive selection could be common in sessile animals, as sessile species are not able to move away from environmental pressures once settled [60]. For Callogorgia occupying this area of the continental slope, variability in temperature and dissolved oxygen may be major factors influencing either larval or post-settlement survival.…”

“…This could lead to selection, and thus adaptive divergence among populations occupying different depths [60]. Pre-reproductive selection could be common in sessile animals, as sessile species are not able to move away from environmental pressures once settled [60].…”

Deepwater Program: Lophelia II, continuing ecological research on deep-sea corals and deep-reef habitats in the Gulf of Mexico

“…Depth can be another important physical factor that drives differentiation in deep-sea species as seen in a chemosynthetic seep mussel genus, Bathymodiolus (Cordes and others, 2007), rockfish (Ingram, 2011), and Caribbean candelabrum coral (Prada and Hellberg, 2013), though often a semipermeable barrier to gene flow (McClain and Hardy, 2010). The average sampling depth in our study ranged from 317 to 642 m. Testing differentiation between samples from their depth range extremes could be useful.…”

“…For example, the E. picta collected from Guadaloupe in the Caribbean belonged only to CLADE II, suggesting that this clade may be more prevalent in this location. Samples from parts of the range of E. picta not included thus far, such as the mid-Atlantic canyons off the U.S. east coast, will also help define ranges of each clade.Depth can be another important physical factor that drives differentiation in deep-sea species as seen in a chemosynthetic seep mussel genus, Bathymodiolus (Cordes and others, 2007), rockfish (Ingram, 2011), and Caribbean candelabrum coral (Prada and Hellberg, 2013), though often a semipermeable barrier to gene flow (McClain and Hardy, 2010). The average sampling depth in our study ranged from 317 to 642 m. Testing differentiation between samples from their depth range extremes could be useful.…”

Inviable immigrants drive diversification in the sea

“…Prada and Hellberg (6) report that E. flexuosa occur as two genetically and morphologically divergent lineages: a shallowwater lineage and a deep-water lineage (Fig. 1A).…”