Divergence genetics analysis reveals historical population genetic processes leading to contrasting phylogeographic patterns in co-distributed species.

Coalescent samplers are computational time machines for inferring the historical demographic genetic processes that have given rise to observable patterns of spatial genetic variation among contemporary populations. We have used traditional characterizations of population structure and coalescent-based inferences about demographic processes to reconstruct the population histories of two co-distributed marine species, the frilled dog whelk, Nucella lamellosa, and the bat star, Patiria miniata. Analyses of population structure were consistent with previous work in both species except that additional samples of N. lamellosa showed a larger regional genetic break on Vancouver Island (VI) rather than between the southern Alexander Archipelago as in P. miniata. Our understanding of the causes, rather than just the patterns, of spatial genetic variation was dramatically improved by coalescent analyses that emphasized variation in population divergence times. Overall, gene flow was greater in bat stars (planktonic development) than snails (benthic development) but spatially homogeneous within species. In both species, these large phylogeographic breaks corresponded to relatively ancient divergence times between populations rather than regionally restricted gene flow. Although only N. lamellosa shows a large break on VI, population separation times on VI are congruent between species, suggesting a similar response to late Pleistocene ice sheet expansion. The absence of a phylogeographic break in P. miniata on VI can be attributed to greater gene flow and larger effective population size in this species. Such insights put the relative significance of gene flow into a more comprehensive historical biogeographic context and have important implications for conservation and landscape genetic studies that emphasize the role of contemporary gene flow and connectivity in shaping patterns of population differentiation.

The 'Expansion-Contraction' model of Pleistocene biogeography: rocky shores suffer a sea change?

Approximately 20,000 years ago the last glacial maximum (LGM) radically altered the distributions of many Northern Hemisphere terrestrial organisms. Fewer studies describing the biogeographic responses of marine species to the LGM have been conducted, but existing genetic data from coastal marine species indicate that fewer taxa show clear signatures of post-LGM recolonization. We have assembled a mitochondrial DNA (mtDNA) data set for 14 co-distributed northeastern Pacific rocky-shore species from four phyla by combining new sequences from ten species with previously published sequences from eight species. Nuclear sequences from four species were retrieved from GenBank, plus we gathered new elongation factor 1-alpha sequences from the barnacle Balanus glandula. Results from demographic analyses of mtDNA for five (36%) species (Evasterias troschelii, Pisaster ochraceus, Littorina sitkana, L. scutulata, Xiphister mucosus) were consistent with large population expansions occurring near the LGM, a pattern expected if these species recently recolonized the region. However, seven (50%) species (Mytilus trossulus, M. californianus, B. glandula, S. cariosus, Patiria miniata, Katharina tunicata, X. atropurpureus) exhibited histories consistent with long-term stability in effective population size, a pattern indicative of regional persistence during the LGM. Two species of Nucella with significant mtDNA genetic structure showed spatially variable demographic histories. Multilocus analyses for five species were largely consistent with mtDNA: the majority of multilocus interpopulation divergence times significantly exceeded the LGM. Our results indicate that the LGM did not extirpate the majority of species in the northeastern Pacific; instead, regional persistence during the LGM appears a common biogeographic history for rocky-shore organisms in this region.

Mechanisms of reproductive isolation among sympatric broadcast-spawning corals of the Montastraea annularis species complex.

Many coral species spawn simultaneously and have compatible gametes, leading to controversy over the nature of species boundaries and the frequency with which hybridization occurs. Three western Atlantic corals, Montastraea annularis, M. faveolata, and M. franksi, typify this controversy; they all spawn sympatrically on the same evenings after the fall full moons. Here we show, in both Panama and the Bahamas for multiple years, how a variety of mechanisms may act in concert to reproductively isolate all three species. Field studies indicate that M. franksi spawns two hours earlier than the other two species, and the eggs released during this earlier period disperse an average of 500 m by the time the other species spawn. Field measures of fertilization indicate that peak fertilization occurs when spawning synchrony is high and that corals that spawn at the tails of the spawning distributions have greatly reduced fertilization success. Laboratory studies indicate that there is a gametic incompatibility between M. faveolata and the other two species. There are regional differences in the gametic compatibility of M. franksi and M. annularis. In Panama, the two species are completely compatible, whereas in the Bahamas, M. franksi sperm can fertilize M. annularis eggs but the reciprocal cross often fails. Gamete age influences patterns of fertilization, such that very young eggs seem resistant to fertilization and old sperm lose viability after two hours. In sum, the combination of temporal differences in spawning, sperm aging, gamete dispersal and dilution, and gametic incompatibility act in various combinations among the three species, making it unlikely that hybrid fertilization would occur.

Plastic reproductive strategies in a clonal marine invertebrate.

Plastic reproductive allocation may allow individuals to maximize their fitness when conditions vary. Mate availability is one condition that may determine the fitness of an individual's allocation strategy. Using a variety of methods, I detected evidence of plastic allocation to asexual (clonal) reproduction in response to mate availability in the brittle star Ophiactis savignyi. There were more mature individuals in populations in which both sexes were present, and clones from these populations had fewer clone-mates than clones from single-sex populations. Animals placed with mates in a field experiment divided less frequently than animals without a mate. These findings demonstrate that animals reduce their allocation to asexual reproduction when mates are present and when a loss of fecundity associated with cloning would decrease offspring production. This plasticity is probably adaptive because it maximizes sexual-reproductive potential when fertilization is more likely, but maximizes survival of the clone when mates are absent and gametes are unlikely to be converted to offspring.

Cryptic species, cryptic endosymbionts, and geographical variation in chemical defences in the bryozoan Bugula neritina.

Molecular markers often offer the only means to discriminate between species and to elucidate the specificity of many community interactions, both of which are key to the understanding of ecological patterns. Western Atlantic populations of the bryozoan Bugula neritina vary in the palatability of their larvae to predators: individuals south of Cape Hatteras produce chemical deterrents to fish predators that are absent in more northern individuals. We use mitochondrial cytochrome oxidase c subunit I (COI) sequences to show that the differences in palatability between populations correlate with the geographical distributions of two cryptic species within B. neritina. Furthermore, these cryptic species differ in their associations with bacteria that may confer chemical resistance to predation. Small subunit rRNA primers specific to a subset of gamma-proteobacteria amplified only the bacterium Endobugula sertula from the southern cryptic species. Endobugula sertula produces a family of chemical compounds (bryostatins) that may deter predators of its animal host. In contrast, the same primers amplified an array of gamma-proteobacteria from the unprotected northern cryptic bryozoan species, but never E. sertula. In combination, these findings suggest that the geographical variation in palatability observed in the larvae of B. neritina is not the result of local adaptation of a single species to regions of differing predation pressure, but rather results from the comparison of cryptic species that differ in the presence or absence of a bacterium that may provide protection against predators. The ability to identify the cryptic Bugula species and their differing relationships with bacterial associates provides an example of the important role molecular techniques may play in addressing ecological questions.

Sex-ratio bias and clonal reproduction in the brittle star Ophiactis savignyi.

Although the sex ratios of many groups conform to Fisher's (1930) prediction that parents should invest equally in daughters and sons, a number of taxa are characterized by excesses of one gender. A variety of mechanisms may lead to sex ratio biases, but in organisms that reproduce clonally as well as sexually, gender differences in the rate of cloning could drive the development of sex-ratio biases. In this study, I demonstrate that males of the clonal brittle star Ophiactis savignyi were significantly more likely to divide than females and that the magnitude of this difference was sufficient to explain the consistent and significant excess of males in natural populations. Females were significantly more likely to lose sexual reproductive capabilities following division, and this greater cost associated with division may explain why females are less likely to divide. Gender differences in mortality rates are unlikely to explain the excess of males in this species. Because of their potential influence on the operational sex ratio, gender differences in division rates may have important ecological and evolutionary implications including effects on the direction and strength of selection.