Molecular phylogeny of echinometrid sea urchins: more species of Heliocidaris with derived modes of reproduction

Abstract

Pachechinus bajulus is an endemic Australian sea urchin with an unusual mode of brooded larval development. We used mitochondrial and nuclear gene sequences to estimate the phylogenetic relationships among Pachechinus and other Echinometridae, including wellstudied species of Heliocidaris with planktonic development. We found strong evidence for the planktotrophic species Heliocidaris tuberculata as the sister group to a clade of three closely related species in which development is known (Heliocidaris erythrogramma, P. bajulus) or suspected (Pachechinus australiae) to be lecithotrophic. Clade support values and likelihood ratio tests rejected monophyly of Heliocidaris species. The sister group to H. erythrogramma is most likely the two Pachechinus species. We resolve the paraphyly problem by reassigning the Pachechinus species to the genus Heliocidaris (the senior synonym), which has six extant species including Heliocidaris australiae and Heliocidaris bajulus. The phylogeny has potentially important implications for comparative studies of developmental morphology and genetics that have assumed a close sister-group relationship between H. erythrogramma and H. tuberculata, and highlights the need for such data from H. bajulus and other Heliocidaris species.Additional key words: Pachycentrotus, bindin, COI, 16S Invertebrate Biology 130(2): 175-185. r

Low Rates of Bindin Codon Evolution in Lecithotrophic Heliocidaris Sea Urchins

“…bajulus , H . australiae)) ; see Hart et al 2011) are consistent with a single transition from small eggs and planktotrophy to large eggs and lecithotrophy (in the common ancestor of H . erythrogramma and H. bajulus ), followed by the evolution of benthic fertilization and the loss of planktonic dispersal in H .…”

“…Here, we test the strength of the association between large evolutionary changes in egg size and large differences in rates of adaptive bindin evolution by extending the original population genetic analyses (McMillan et al 1992;Zigler et al 2003) of Heliocidaris sea urchins to include a second lecithotrophic species, H. bajulus (in which eggs are fertilized on the female and brooded by her without planktonic dispersal of larvae). Phylogenetic relationships among four Heliocidaris species (H. tuberculata, (H. erythrogramma, (H. bajulus, H. australiae)); see Hart et al 2011) are consistent with a single transition from small eggs and planktotrophy to large eggs and lecithotrophy (in the common ancestor of H. erythrogramma and H. bajulus), followed by the evolution of benthic fertilization and the loss of planktonic dispersal in H. bajulus (Fig. 1).…”

“…We tested the prediction that rates of adaptive bindin evolution in H. bajulus are similar to the previously reported high rate of bindin codon evolution in the closely related H. erythrogramma with which it shares large egg size as a synapomorphy (Zigler et al 2003;Hart et al 2011) (Fig. 1).…”

“…We sequenced the mitochondrial cytochrome c oxidase subunit I protein-coding gene (COI, partial coding sequence, about 700 bp) and the nuclear locus for bindin (complete coding sequence, about 1300 bp). We used polymerase chain reaction (PCR), cloning, and sequencing methods described in detail elsewhere (Hart et al 2011). We sequenced 20 COI haplotypes (11 from Clyde Island, nine from Bruny Island) and 26 bindin alleles (16 from Clyde Island, 10 from Bruny Island, including two Bruny Island homozygotes).…”

Population Dynamics of Edible Sea Urchins Associated with Variability of Seaweed Beds in Northern Japan

“…In Japan, the six species of sea urchins Mesocentrotus nudus (nee Strongylocentrotus nudus) (Tatarenko and Poltaraus 1993), Strongylocentrotus intermedius, Hemicentrotus pulcherrimus, Pseudocentrotus depressus, Heliocidaris crassispina and Tripneustes gratilla are commercially harvested. Heliocidaris crassispina has been studied as Anthocidaris crassispina, but Anthocidaris is considered a junior synonym of Heliocidaris (Hart et al 2011). The total catches (whole weight) decreased from 23 000 metric tons in 1987 to 7 881 metric tons in 2011 (Fig.…”