Evolution of Poecilogony and the Biogeography of North American Populations of the Polychaete Streblospio

Abstract

Invertebrate interspecific developmental patterns can be highly variable and, taxonomically, are considered only weakly constrained. Intraspecifically, some invertebrate species possess multiple developmental modes-a condition known as poecilogony. Closer examination of most putative poecilogenous species, however, has not supported poecilogony, but rather has uncovered hidden or cryptic species. The polychaete Streblospio benedicti is a well-known, poecilogenous species found along the coast of North America. We collected mitochondrial cytochrome subunit I DNA sequence data from 88 individuals taken from 11 locations along the Atlantic, Gulf, and Pacific Coasts of the United States to provide a phylogenetic framework from which to interpret intraspecific variation in larval life history and brooding structure morphology in this species. Our results are consistent with a recent revision of the species into two separate species: S. benedicti, a pouched brooding form distributed along the Atlantic and Pacific Coasts, and S. gynobranchiata, a branchiate brooding form in the Gulf of Mexico. Contrary to the redescription, S. benedicti is paraphyletic because the pouched brooding population in Vero Beach, Florida shows strong genetic affinity with Gulf of Mexico populations (S. gynobranchiata). However, S. benedicti is a true poecilogenous species, with both lecithotrophic and planktotrophic individuals possessing identical mitochondrial DNA haplotypes. Crossbreeding experiments further support the molecular phylogeny with reproductive isolation demonstrated between, but not within, the major phylogenetic clades consistent with the previously described species. The genetic break near Vero Beach, Florida, corresponds to a well-known phylogeographic boundary, but the estimated time of separation for the Streblospio spp., approximately 10 million years before present, predates all other known phylogeographic subdivisions in this area. This suggests that biogeographic sundering in this region is a recurrent event. Divergence times within the major Streblospio spp. clades are recent and indicate that changes in larval life history as well as brooding structure morphology are highly plastic and can evolve rapidly.

Molecular systematics of polychaetes (Annelida)

“…In this case, the authors used COI sequences to hypothesize relationships among populations of Streblospio, a polychaete group known to exhibit poecilogony, i.e., the presence of more than one developmental mode within a species. Maximum parsimony and distance analyses of 88 sequences from individuals of S. benedicti and S. gynobranchiata along the east and west coasts of North America supports paraphyly of S. benedicti with respect to S. gynobranchiata, and also corroborates poecilogony in this group (Schulze et al, 2000). Using molecular clock estimates of divergence times, Schulze et al (2000) proposed that divergence times among clades of Streblospio are recent and thus the evolutionary changes in larval developmental modes have been rapid.…”

“…While the basal relationships among the ingroup taxa were not resolved, the resulting trees allowed the inference that the reproductive mode of Ophryotrocha changed once and that simultaneous hermaphroditism is the reproductive mode of the immediate ancestor to the sequential hermaphroditic Ophryotrocha clade (Dahlgren et al, 2001). Schulze et al (2000) were also interested in the evolution of reproductive modes in a polychaete group. In this case, the authors used COI sequences to hypothesize relationships among populations of Streblospio, a polychaete group known to exhibit poecilogony, i.e., the presence of more than one developmental mode within a species.…”

Discrete genetic boundaries of threeStreblospio(Spionidae, Annelida) species and the status ofS. shrubsolii

“…A range of developmental modes associated with brooding occur in Streblospio including (1) release of planktotophic larvae, (2) release of lecithotrophic larvae, (3) direct development and (4) poecilogony (Levin 1984;Levin et al 1991;Levin & Bridges 1995;Schulze et al 2000).…”

“…Occurrences of S. benedicti from the Pacific coast of North America and from the North Atlantic coast of Europe are generally considered to represent introductions (Carlton 1979;Fonseca-Genevois & Cazaux 1987;Schulze et al 2000). Streblospio shrubsolii was originally described from the northern coast of England (Buchanan 1890) and is recorded from the Mediterranean, the Atlantic coast of Europe, and the Baltic Sea (see Dauer et al 2003).…”

“…The third species, Streblospio gynobranchiata, was originally described from the Gulf of Mexico and southern Florida and is morphologically indistinct from S. benedicti except in reproductive females (Rice & Levin 1998;Schulze et al 2000). Recent reports of S. gynobranchiata in the eastern Mediterranean Sea have been attributed to an introduction, most likely through ballast water release (Ç inar et al 2005, 2006).…”