Fine-scale patterns of genetic divergence within and between morphologically variable subspecies of the sea urchin Heliocidaris erythrogramma (Echinometridae)

Abstract

The spatial scale over which genetic divergences occur between populations and the extent that they are paralleled by morphological differences can vary greatly among marine species. In the present study, we use a hierarchical spatial design to investigate genetic structure in Heliocidaris erythrogramma occurring on near shore limestone reefs in Western Australia. These reefs are inhabited by two distinct subspecies: the thick-spined Heliocidaris erythrogramma armigera and the thin-spined Heliocidaris erythrogramma erythrogramma, each of which also have distinct colour patterns. In addition to pronounced morphological variation, H. erythrogramma exhibits a relatively short (3-4 days) planktonic phase before settlement and metamorphosis, which limits their capacity for dispersal. We used microsatellite markers to determine whether patterns of genetic structure were influenced more by morphological or life history limitations to dispersal. Both individual and population-level analyses found significant genetic differentiation between subspecies, which was independent of geographical distance. Genetic diversity was considerably lower within H. e. erythrogramma than within H. e. armigera and genetic divergence was four-fold greater between subspecies than among populations within subspecies. This pattern was consistent even at fine spatial scales (< 5 km). We did detect some evidence of gene flow between the subspecies; however, it appears to be highly restricted. Within subspecies, genetic structure was more clearly driven by dispersal capacity, although weak patterns of isolation-by-distance suggest that there may be other factors limiting gene exchange between populations. Our results show that spatial patterns of genetic structure in Western Australian H. erythrogramma is influenced by a range of factors but is primarily correlated with the distribution of morphologically distinct subspecies. This suggests the presence of reproductive barriers to gene exchange between them and demonstrates that morphological variation can be a good predictor of genetic divergence.

Oceanic circulation, local upwelling and palaeoclimatic changes linked to the phylogeography of the Cape sea urchin Parechinus angulosus

“…This lack of congruence between the genetic data and the colour morphs is in line with previous echinoid studies (Boissin et al 2008, Vardaro 2010; but see Calderón et al 2010, Binks et al 2011. Since individuals of different colours are often found in the same pools, it seems reasonable to conclude that mating and fertilization between colour morphs is indiscriminate.…”

Low Rates of Bindin Codon Evolution in Lecithotrophic Heliocidaris Sea Urchins

“…tuberculata (with small eggs). Population‐level bindin variation in H. bajulus was similar to population variation at other loci (mtDNA, microsatellites) that have previously been used to assess population structure in Heliocidaris (McMillan et al 1992; Binks et al 2009, 2011). High rates of nonsynonymous bindin substitution appear to be restricted to a small number of codons in H .…”

“…Differentiation based on microsatellite allele frequencies also varied between loci: stronger ( F ST = 0.115) and significant ( P = 0.035) for HerC10, negligible ( F ST =−0.001) and not significant ( P = 0.294) for HerC101. The average fixation index across all four loci ( F ST = 0.076) was higher than average microsatellite pairwise F ST on a similar spatial scale (<100 km) for populations of H. erythrogramma in Western Australia ( F ST ∼0.02; Binks et al 2011).…”

“…We found instead that bindin evolution in H. bajulus is characterized by purifying selection and low rates of amino acid substitution similar to the background rate for other species, including H. tuberculata . Our phylogeographic analysis of bindin and other genetic markers (not involved in gamete recognition) shows that this unexpected pattern of bindin evolution occurs in a demographic context—significant population genetic differentiation on relatively small spatial scales <100 km—that is typical of sea urchins and other marine invertebrates with limited larval dispersal potential (Bohonak 1999; Weersing and Toonen 2009), including species such as H. erythrogramma with brief planktonic development (Binks et al 2011). Given this phylogeographic context, it seems unlikely that the difference in bindin divergence between H. bajulus and H. erythrogramma is driven by some unusual demographic process in H. bajulus , and instead reflects some aspect of selection acting on H. bajulus bindin that differs from H .…”

More Than Bindin Divergence: Reproductive Isolation Between Sympatric Subspecies of a Sea Urchin by Asynchronous Spawning

“…To strengthen these two analyses, we combined the mitochondrial data from this study with microsatellite data; all Western Australian microsatellite data were acquired from a previous study (Binks et al 2011b) whereas Eastern Australian data were obtained by amplifying individuals collected in the current study with the methods described in Binks et al (2011b). Thus, both analyses were run with a total of five loci; CO1 and 16S ( n A = 32, n B = 44 for each locus) were run under the Hasegawa‐Kishino‐Yano (HKY) mutational model and all three microsatellite loci (C101, C115, and D105) were run under the stepwise mutational model using a subsample of randomly selected individuals ( n A = 378, n B = 268 for each locus).…”