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Tethyan vicariance, relictualism and speciation: evidence from a global molecular phylogeny of the opisthobranch genus Bulla

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Abstract Aim 

Our aims were: (1) to reconstruct a molecular phylogeny of the cephalaspidean opisthobranch genus Bulla, an inhabitant of shallow sedimentary environments; (2) to test if divergence times are consistent with Miocene and later vicariance among the four tropical marine biogeographical provinces; (3) to examine the phylogenetic status of possible Tethyan relict species; and (4) to infer the timing and causes of speciation events. Location 

Tropical and warm-temperate regions of the Atlantic, Indo-West Pacific, Australasia and eastern Pacific. Methods 

Ten of the 12 nominal species of Bulla were sampled, in a total sample of 65 individuals, together with cephalaspidean outgroups. Phylogenetic relationships were inferred by Bayesian analysis of partial sequences of the mitochondrial cytochrome c oxidase I (COI) and 16S rRNA and nuclear 28S rRNA genes. Divergence times and rates of evolution were estimated using uncorrelated relaxed-clock Bayesian methods with fossil calibrations (based on literature review and examination of fossil specimens), implemented inbeast. The geographical pattern of speciation was assessed by estimating the degree of overlap between sister lineages. Results 

Four clades were supported: Indo-West Pacific (four species), Australasia (one species), Atlantic plus eastern Pacific (three species) and Atlantic (two species), with estimated mean ages of 35–46 Ma. Nominal species were monophyletic, but deep divergences were found within one Indo-West Pacific and one West Atlantic species. Species-level divergences occurred in the Miocene or earlier. The age of a sister relationship across the Isthmus of Panama was estimated at 7.9–32.1 Ma, and the divergence of a pair of sister species on either side of the Atlantic Ocean occurred 20.4–27.2 Ma. Main conclusions 

Fossils suggest that Bulla originated in the Tethys realm during the Middle Eocene. Average ages of the four main clades fall in the Eocene, and far pre-date the 18–19 Ma closure of the Tethys Seaway. This discrepancy could indicate earlier vicariant events, selective extinction or errors of calibration. Similarly, the transisthmian divergence estimate far pre-dates the uplift of the Panamanian Isthmus at about 3 Ma. Speciation events occurred in the Miocene, consistent with tectonic events in the central Indo-West Pacific, isolation of the Arabian Sea by upwelling and westward trans-Atlantic dispersal. Differences in habitat between sister species suggest that ecological speciation may also have played a role. The basal position of the Australasian species supports its interpretation as a Tethyan relict.
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Keywords: Allopatry; Bulla; Tethys; dispersal; diversification; relict species; speciation; uncorrelated relaxed-clock; vicariance

Document Type: Research Article

Affiliations: Department of Zoology, Natural History Museum, London, UK

Publication date: September 1, 2009

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