Genetic diversity and demographic instability in Riftia pachyptila tubeworms from eastern Pacific hydrothermal vents

Abstract

Background: Deep-sea hydrothermal vent animals occupy patchy and ephemeral habitats supported by chemosynthetic primary production. Volcanic and tectonic activities controlling the turnover of these habitats contribute to demographic instability that erodes genetic variation within and among colonies of these animals. We examined DNA sequences from one mitochondrial and three nuclear gene loci to assess genetic diversity in the siboglinid tubeworm, Riftia pachyptila, a widely distributed constituent of vents along the East Pacific Rise and Galápagos Rift.

Results: Genetic differentiation (F(ST)) among populations increased with geographical distances, as expected under a linear stepping-stone model of dispersal. Low levels of DNA sequence diversity occurred at all four loci, allowing us to exclude the hypothesis that an idiosyncratic selective sweep eliminated mitochondrial diversity alone. Total gene diversity declined with tectonic spreading rates. The southernmost populations, which are subjected to superfast spreading rates and high probabilities of extinction, are relatively homogenous genetically.

Conclusions: Compared to other vent species, DNA sequence diversity is extremely low in R. pachyptila. Though its dispersal abilities appear to be effective, the low diversity, particularly in southern hemisphere populations, is consistent with frequent local extinction and (re)colonization events.

Figure 1

Habitat instability and genetic diversity in R. pachyptila. (A) A healthy patch of tubeworms at the N27 locality. (B) An adjacent senescent patch on a rust-colored sulfide mound covered with numerous scavengers, the galatheid squat lobster Munidopsis subsquamosa. (C) Riftia pachyptila samples: blue and red dots indicate northern and southern sample locations; gray dots indicate active vents known to host R. pachyptila but not included in present analyses; white dots denote active vents that did not host substantial R. pachyptila colonies during the times of our expeditions; and white diamonds denote vents that did not support R. pachyptila colonies. Tectonic spreading rates are indicated along arrows for each location. (D) Allelic frequencies at four loci. Colors are coded to adjacent haplotype networks (black wedges are singletons). (E) Structure plots for the mean probability of assignment of individuals (Q values) to the northern cluster (blue) versus the southern cluster (white). (F) Haplotype networks for six genetic markers. Area of circle is proportional to the frequency of each haplotype, and straight lines denote single nucleotide differences.

Figure 2

Correlation of genetic differentiation with geographic distances among eight sample localities. Negative values for F_ST (Table 3) were set to zero prior to adjustment. Black dots denote contrasts between populations from the northern and southern clusters. White dots denote contrasts within clusters.

Figure 3

Correlation of expected heterozygosity with tectonic spreading rates (R² = 0.788, P = 0.0032). Allelic richness exhibits essentially the same relationship (R² = 0.730, P = 0.0069). Black squares are NEPR populations, white squares are SEPR samples and the white circle is the GAR population.