Flying shells: historical dispersal of marine snails across Central America

Abstract

The geological rise of the Central American Isthmus separated the Pacific and the Atlantic oceans about 3 Ma, creating a formidable barrier to dispersal for marine species. However, similar to Simpson's proposal that terrestrial species can 'win sweepstakes routes'-whereby highly improbable dispersal events result in colonization across geographical barriers-marine species may also breach land barriers given enough time. To test this hypothesis, we asked whether intertidal marine snails have crossed Central America to successfully establish in new ocean basins. We used a mitochondrial DNA genetic comparison of sister snails (Cerithideopsis spp.) separated by the rise of the Isthmus. Genetic variation in these snails revealed evidence of at least two successful dispersal events between the Pacific and the Atlantic after the final closure of the Isthmus. A combination of ancestral area analyses and molecular dating techniques indicated that dispersal from the Pacific to the Atlantic occurred about 750 000 years ago and that dispersal in the opposite direction occurred about 72 000 years ago. The geographical distribution of haplotypes and published field evidence further suggest that migratory shorebirds transported the snails across Central America at the Isthmus of Tehuantepec in southern Mexico. Migratory birds could disperse other intertidal invertebrates this way, suggesting the Central American Isthmus may not be as impassable for marine species as previously assumed.

Figure 1.

Molecular phylogeny and geographical distribution of the intertidal snails, Cerithideopsis californica and C. pliculosa. A maximum-likelihood tree was constructed based on 873 bp of the CO1 gene. The major clades are categorized as clades A, B and the detailed subclades are within. Numbers near nodes are the support values for the clade from the different analyses (ML/BI). The scale bar represents the phylogenetic distances expressed as units of expected nucleotide substitutions per site. Phylogenetic relationships within the clades are shown in electronic supplementary material, figure S1. The distributions of the major genetic clades are shown at the right side of the figure. Numbers near the geographical points indicate sample size. Letters indicate sampling sites (see electronic supplementary material, table S1).

Figure 2.

Divergence time estimates for the major clades in C. californica and C. pliculosa based on the CO1, 16S, 12S, Cytb and ND6 genes (totally 2952 bp). Horizontal bars represent the upper and lower interval bounds for 95% of the highest posterior densities (HPDs). Each gene tree is shown in electronic supplementary material, figure S2.

Figure 3.

Mitochondrial haplotype networks of Cerithideopsis californica and C. pliculosa, subclades A1 and A2 (a), and subclade B1 (b) based on the CO1 gene. Circle sizes are proportional to the number of individuals observed for each haplotype. The small black circles represent unobserved single-nucleotide substitutions. The pie chart coloration/shading indicates the regions where haplotypes were collected (see electronic supplementary material, table S1).