EVOLUTIONARY HISTORY OF NORTHERN HEMISPHERE NUCELLA (GASTROPODA, MURICIDAE): MOLECULAR, MORPHOLOGICAL, ECOLOGICAL, AND PALEONTOLOGICAL EVIDENCE.

By combining data from a variety of sources we explore patterns of evolution and speciation in Nucella, a widely studied genus of shallow-water marine neogastropods. We present a hypothesis of phylogenetic relationships for all of the currently recognized species of northern hemisphere Nucella, based on an analysis of 718 base pairs of nucleotide sequence from the mitochondrial cytochrome b gene. The order of appearance of species in the fossil record is congruent with this hypothesis. The topology of the inferred phylogeny of Nucella, coupled with ecological, morphological, and fossil evidence, was used to address three main questions: (1) At what time and by which route was the North Atlantic invaded from the North Pacific compared to prior studies of the trans-Arctic interchange? (2) Do patterns of molecular variation within species corroborate the importance of climatic cycles in driving speciation in north temperate marine animals? (3) Was radiation in the direction of increased or decreased ecological specialization, body size, or vulnerability to predation? Molecular evidence confirmed that the sole North Atlantic species, N. lapillus, arose from a North Pacific ancestor. Biogeographic and paleontological evidence supported the dispersal of Nucella, and perhaps other interchange species, via the Eurasian Arctic. Rather intriguingly, the linkage of N. lapillus to a western as opposed to eastern Pacific clade, and the biogeographic origins of the eastern Pacific species, parallel closely similar patterns observed in another genus of rocky-shore gastropods, Littorina. This congruence, in conjunction with information on the climatic and geographic histories of the region, as well as the geographic arrangement of mtDNA haplotypes within Nucella species, supports a model of speciation in Nucella driven by cycles of climatic amelioration and deterioration that began during the Miocene. Calibrations from the fossil record of Nucella suggest that third position transitions and transversions accrue at a rate of 3-4% and 0.5% respectively per million yr. This supports an early participation by Nucella in the trans-Arctic interchange, as suggested by paleobiogeographic studies. Consistent with the unstable taxonomic history of species of Nucella, we found few nonmolecular traits to be phylogenetically informative. Among North Pacific species, more recently derived species (N. canaliculata and the N. emarginata clade) were more ecologically specialized (narrower diet and habitat range). Consistent with extensive intraspecific variation, shell traits were quite labile evolutionarily: neither overall size nor development of antipredatory traits exhibited consistent evolutionary trends over the history of the genus. Nurse eggs (unfertilized eggs consumed by developing embryos) were an ancestral trait that was lost evolutionarily in the two clades that also exhibited increased body size, suggesting that these two life-history traits may be coupled. The reduced number of chromosomes in N. lapillus is clearly a derived state and is consistent with White's (1978) observations on chromosome evolution in other clades.