DNA sequence evidence for speciation, paraphyly and a Mesozoic dispersal of cancellothyridid articulate brachiopods

Abstract

Abstract.Because the classification of extant and fossil articulate brachiopods is based largely upon shell characters observable in fossils, it identifies morphotaxa whose biological status can, in practice, best be inferred from estimates of genetic divergence. Allozyme polymorphism and restriction fragment length polymorphism of mitochondrial DNA (mtDNA RFLP) have been used to show that nuclear and mitochondrial genetic divergence between samples of the cancellothyridid brachiopods Terebratulina septentrionalis from Canada and T. retusa from Europe is compatible with biological speciation, but the genetic distances obtained were biased by methodological limitations. Here, we report estimates of divergence in 12S rDNA mitochondrial sequences within and between samples of these brachiopods. The sequence-based genetic distance between these samples (5.98 ± s.e.m. 0.07%) is at least ten times greater than within them and, since they also differ in a complex life-history trait, their species status is considered to be securely established.Divergence levels between 12S rDNA genes of three other cancellothyridids, Terebratulina unguicula from Alaska, T. crossei from near Japan, and Cancellothyris hedleyi from near Australia are higher than between the two North Atlantic species, and the mean nucleotide distance between all these cancellothyrids is similar to the mean distance between species of Littorina (Mollusca: Gastropoda). Sequences of both 12S and 16S genes from cancellothyridids and other short-looped brachiopod species show neither saturation nor lineagespecific rate differences and, when analysed with different outgroups, either separately or together, yield one unexpected, but well-supported, tree with Alaskan T. unguicula basal and C. hedleyi nested within Terebratulina, i.e. these genera are paraphyletic. A geologically dated divergence between Antarctic and New Zealand species of the short-looped brachiopod Liothyrella is used to calibrate the rate of 12S evolution at ca. 0.1% per MY, and this rate is used to infer that T. septentrionalis and T. retusa have been diverging for ca.60 MY and that they and T. unguicula have been diverging from their last common ancestor for ca. 100 MY.

Detecting hybridization between sister species of Terebratulina (Brachiopoda, Cancellothyridoidea) in the North Atlantic: morphology versus molecules

“…Curry & Endo 16 , unable to find such cline in their data, concluded that hybrids do not exist and that their morphometric approach clearly discriminated between two Atlantic species of Terebratulina . This was also confirmed by allozyme data and mitochondrial RFLP analysis 21 and by sequence analyses of mitochondrial DNA 7 .…”

“…As has been shown in a previous study 7 , the molecular markers used here are highly conserved intraspecifically, i.e. identification of either T. retusa or T. septentrionalis is possible based on sequence information alone.…”

“…This might be the reason for T. septentrionalis being absent altogether from the records in the Paleobiology Database 46 . With regard to the unusually high longevity of 60 MY of the two species according to a previous molecular clock approach 7 , the fossil record is, therefore, not suitable to reconstruct the speciation history and palaeogeographic distribution of Terebratulina species in the North Atlantic.…”

“…Sequence alignments of both mitochondrial and nuclear markers were compared between specimens based on single bp comparison across their entire length. This method yielded robust data for species identification even when comparing Terebratulina populations across large spatial scales 7 . For PCR primers used see Supplementary Table S3.…”

“…According to molecular phylogenies T. retusa and T. septentrionalis in a comprehensive study on molecular systematics of cancellothyridid brachiopods 7 were found to be sister species resulting from an allopatric speciation event during the Early Paleogene about 60 MYA, which became possible after the opening of the North Atlantic. Whereas T. retusa was originally described from Scandinavian waters by Linné 8 , the morphologically similar T. septentrionalis was first mentioned in Couthouy’s account on new molluscs from New England’s coast 9 .…”