Thermal selection as a driver of marine ecological speciation

Abstract

Intraspecific genetic structure in widely distributed marine species often mirrors the boundaries between temperature-defined bioregions. This suggests that the same thermal gradients that maintain distinct species assemblages also drive the evolution of new biodiversity. Ecological speciation scenarios are often invoked to explain such patterns, but the fact that adaptation is usually only identified when phylogenetic splits are already evident makes it impossible to rule out the alternative scenario of allopatric speciation with subsequent adaptation. We integrated large-scale genomic and environmental datasets along one of the world's best-defined marine thermal gradients (the South African coastline) to test the hypothesis that incipient ecological speciation is a result of divergence linked to the thermal environment. We identified temperature-associated gene regions in a coastal fish species that is spatially homogeneous throughout several temperature-defined biogeographic regions based on selectively neutral markers. Based on these gene regions, the species is divided into geographically distinct regional populations. Importantly, the ranges of these populations are delimited by the same ecological boundaries that define distinct infraspecific genetic lineages in co-distributed marine species, and biogeographic disjunctions in species assemblages. Our results indicate that temperature-mediated selection represents an early stage of marine ecological speciation in coastal regions that lack physical dispersal barriers.

Keywords: adaptation; dispersal barrier; ecological speciation; marine biogeography; seascape genomics; thermal selection.

Figure 1.

Sampling sites, marine bioregions, and examples of genetic breaks in South African coastal animals; (a) a map indicating the location of sampling sites within southern Africa's temperature-defined marine bioregions; (b) maximum and minimum sea surface temperatures (SSTs) at each sampling site; these temperatures divide bioregions into two groups each (indicated by ellipses), and by themselves only partially explain the region's biogeography; (c) examples of distribution ranges (grey horizontal bars) and location of genetic breaks (black vertical bars) in coastal South African animals, arranged hierarchically. (i) Species that occur as a single phylogenetic lineage in multiple bioregions: 1, Psammogobius knysnaensis (the study species, marked with an asterisk) [7] and 2, Scutellastra longicosta [8]. (ii) Species with phylogenetically distinct sister lineages that are not distinguishable morphologically (cryptic species): 3, Callichirus kraussi [9] and 4, Palaemon peringueyi [10]. (iii) Morphologically distinguishable sister species: 5, Hymenosoma spp. [11] and 6, Tricolia spp. [12]. W, cool-temperate west coast; SW, transition zone on the southwest coast; S, warm-temperate south coast; SE, transition zone on the southeast coast; E, subtropical east coast.

Figure 2.

Population genetic structure inferred for temperature-associated loci, and reconstruction of phylogenetic relationships between individuals of Psammogobius knysnaensis from four South African marine bioregions; (a) DAPC compoplot for minimum SST data using geography as the covariate (results for alternative combinations of temperature data and covariates are shown in electronic supplementary material, figure S4); (b) corresponding consensus fastStructure barplot for four genetic clusters (K) (for comparison, barplots for K = 2–5 are shown in electronic supplementary material, figure S5); (c) MCC tree of 218 sequences from phased SNP data (same as in a and b), with location state reconstructions of ancestral nodes; and d corresponding phylogenetic tree based on mtDNA COI data [7]. In c, clear regional structure is evident, but there are possible migrants. The south coast cluster was identified as being the oldest. By contrast, there are no clear regional clades in d, and there was no evidence for any cluster being the oldest. Site numbers and abbreviations correspond to those in figure 1 and electronic supplementary material, table S1, and trees are not drawn to scale.