Determining gene flow and the influence of selection across the equatorial barrier of the East Pacific Rise in the tube-dwelling polychaete Alvinella pompejana

Abstract

Background: Comparative phylogeography recently performed on the mitochondrial cytochrome oxidase I (mtCOI) gene from seven deep-sea vent species suggested that the East Pacific Rise fauna has undergone a vicariant event with the emergence of a north/south physical barrier at the Equator 1-2 Mya. Within this specialised fauna, the tube-dwelling polychaete Alvinella pompejana showed reciprocal monophyly at mtCOI on each side of the Equator (9 degrees 50'N/7 degrees 25'S), suggesting potential, ongoing allopatric speciation. However, the development of a barrier to gene flow is a long and complex process. Secondary contact between previously isolated populations can occur when physical isolation has not persisted long enough to result in reproductive isolation between genetically divergent lineages, potentially leading to hybridisation and subsequent allelic introgression. The present study evaluates the strength of the equatorial barrier to gene flow and tests for potential secondary contact zones between A. pompejana populations by comparing the mtCOI gene with nuclear genes.

Results: Allozyme frequencies and the analysis of nucleotide polymorphisms at three nuclear loci confirmed the north/south genetic differentiation of Alvinella pompejana populations along the East Pacific Rise. Migration was oriented north-to-south with a moderate allelic introgression between the two geographic groups over a narrow geographic range just south of the barrier. Multilocus analysis also indicated that southern populations have undergone demographic expansion as previously suggested by a multispecies approach. A strong shift in allozyme frequencies together with a high level of divergence between alleles and a low number of 'hybrid' individuals were observed between the northern and southern groups using the phosphoglucomutase gene. In contrast, the S-adenosylhomocysteine hydrolase gene exhibited reduced diversity and a lack of population differentiation possibly due to a selective sweep or hitch-hiking.

Conclusions: The equatorial barrier leading to the separation of East Pacific Rise vent fauna into two distinct geographic groups is still permeable to migration, with a probable north-to-south migration route for A. pompejana. This separation also coincides with demographic expansion in the southern East Pacific Rise. Our results suggest that allopatry resulting from ridge offsetting is a common mechanism of speciation for deep-sea hydrothermal vent organisms.

Figure 1

Map of the south-east Pacific and Alvinella pompejana sampling locations along the East Pacific Rise. Dots represent sampled hydrothermal vent fields. The bracket between 9°50'N and 7°25'S indicates the Quebrada, Discovery and Gofar transform faults from north to south, respectively.

Figure 2

Allozyme frequency clines along the East Pacific Rise. Frequencies of the most frequent alleles found in A. pompejana populations for PGM, MPI, TPI, HK and 6PGD allozyme loci are plotted according to latitude. Each colour represents a distinct allozyme locus. Individuals from 9°50'N were not used in the analysis simply because they have been only preserved in alcohol.

Figure 3

Median-joining networks of the mtCOI and nuclear genes. Blue and red labels represent individuals sampled from the northern (9°50'N and 13°N) and southern (7°25'S-21°33'S) EPR, respectively. Sizes of haplotype circles and lengths of connecting lines are proportional to the number of sequences studied and the number of mutations that separate two linked haplotypes, respectively. Nuclear genes are rooted by a consensus outgroup sequence of A. caudata (connecting line between A. pompejana and the A. caudata outgroup is not representative of sequence differences due to the high number of mutations).

Figure 4

Marginal posterior probability distribution for parameters estimated by the isolation-with-migration model. Marginal posterior probabilities are estimated for (A) divergence time between the northern and southern EPR, (B) the forward-in-time migration rates between the northern and southern EPR, where m_s represents south-to-north migration and m_n north-to-south and (C) effective population sizes of the ancestral population (N_a) and the two sister populations (i.e. N_n and N_s for the northern EPR population and the southern EPR population, respectively). Values estimated using IMa and 90% highest posterior density intervals of these parameters are presented in additional file 4.

Figure 5

Ultrametric neighbour-joining topologies of four genes in A. pompejana in the northern and southern EPR. The outgroup A. caudata (dotted lines) was used to root the phylogenetic trees that were constructed from the most well-aligned parts of the four studied genes.

Figure 6

Sensitivity of RFLP and allozyme PGM markers for detecting the equatorial genetic break. The distance θ is plotted against the geographic distance between hydrothermal vent localities. The RFLP dataset shows a clearer departure from the isolation-by-distance model's expectation, indicating that markers to better detect the equatorial genetic break.