Thomas J. Hilbish

THE GEOGRAPHY OF MARINE LARVAL DISPERSAL: COUPLING GENETICS WITH FINE-SCALE PHYSICAL OCEANOGRAPHY

Efforts to understand the population dynamics of marine species with planktonic larvae have been stymied by the fact that the larvae recruiting to a location have little chance of originating from that site. Patterns of larval movement and the spatial scale of dispersal are expected to be major forces regulating the dynamics of marine populations and communities. Unfortunately, the scale and predictability of larval dispersal and its regulation by physical circulation remains unknown due largely to the impossibility of measuring dispersal in open marine environments. Here we exploit strong genetic differentiation among marine mussel populations in southwest England to measure larval dispersal among adjoining genetic patches. This approach allows estimates of larval dispersal over relatively great distances. We combine these measurements with results from a high-resolution model of coastal circulation to test the hypothesis that larval dispersal is regulated by physical circulation. We show that larval dispersal typically occurs over distances of ∼30 km but in some cases was at least 64 km. The circulation model accurately predicted general patterns of larval transport between genetic regions, the scale of larval dispersal, and genetic isolation created by physical barriers to circulation. We demonstrate that physical circulation models and genetic measures of larval transport can be coupled to assess the geographic scale of larval dispersal in marine environments.

TEMPORAL VARIATION IN THE REPRODUCTIVE CYCLE OF MYTILUS EDULIS L. (BIVALVIA, MYTILIDAE) FROM LOCALITIES ON THE EAST COAST OF THE UNITED STATES

The reproductive condition of seven latitudinally separated populations of the mussel Myti!us edu!is on the east coast of the United States was determined using histological analysis and stereology. Differences in the timing of various phases of the gametogenic cycle among populations did not have any discernible latitudinal trend. Two populations at the same latitude on Long Island, N. Y. had the greatest temporal differences observed in gametogenic cycle, with summer reproduction maxima separated by a 3-month interval. There was no difference in the water temperature regime between these two habitats and thus the rate of gametogenic development was not a constant function of temperature. The observed differences in the gametogenic cycle were attributed to temporal and quantitative differences between habitats in the energy content of the mussels food supply.

Evidence for intragenic recombination within a novel genetic marker that distinguishes mussels in the Mytilus edulis species complex

We have used the polymerase chain reaction (PCR) and restriction fragment length polymorphism (RFLP) techniques to design two genetic markers for blue mussels in the Mytilus edulis species complex. Both of these markers target the gene encoding the mussel polyphenolic adhesive protein. The first marker, Glu-5′, is highly differentiated among and can be used to identify the three blue mussel species, M. edulis, M. galloprovincialis and M. trossulus. The second marker, Glu-3′, can identify M. edulis and M. galloprovincialis. Using these markers we have demonstrated that hybrid mussels from Whitsand Bay, UK carry alleles for this gene that are the products of intragenic recombination. The high frequency (10 per cent) of these recombinant alleles within the hybrid population suggests that recombination is fairly frequent within this gene or that hybridization between M. edulis and M. galloprovincialis is substantial and has been occurring over considerable evolutionary time. The two novel genetic markers, Glu-5′ and Glu-3′ will be invaluable in additional studies regarding the importance of hybrization among blue mussels.

Ecological genetics in the North Atlantic: environmental gradients and adaptation at specific loci.

The North Atlantic intertidal community provides a rich set of organismal and environmental material for the study of ecological genetics. Clearly defined environmental gradients exist at multiple spatial scales: there are broad latitudinal trends in temperature, meso-scale changes in salinity along estuaries, and smaller scale gradients in desiccation and temperature spanning the intertidal range. The geology and geography of the American and European coasts provide natural replication of these gradients, allowing for population genetic analyses of parallel adaptation to environmental stress and heterogeneity. Statistical methods have been developed that provide genomic neutrality tests of population differentiation and aid in the process of candidate gene identification. In this paper, we review studies of marine organisms that illustrate associations between an environmental gradient and specific genetic markers. Such highly differentiated markers become candidate genes for adaptation to the environmental factors in question, but the functional significance of genetic variants must be comprehensively evaluated. We present a set of predictions about locus-specific selection across latitudinal, estuarine, and intertidal gradients that are likely to exist in the North Atlantic. We further present new data and analyses that support and contradict these simple selection models. Some taxa show pronounced clinal variation at certain loci against a background of mild clinal variation at many loci. These cases illustrate the procedures necessary for distinguishing selection driven by internal genomic vs. external environmental factors. We suggest that the North Atlantic intertidal community provides a model system for identifying genes that matter in ecology due to the clarity of the environmental stresses and an extensive experimental literature on ecological function. While these organisms are typically poor genetic and genomic models, advances in comparative genomics have provided access to molecular tools that can now be applied to taxa with well-defined ecologies. As many of the organisms we discuss have tight physiological limits driven by climatic factors, this synthesis of molecular population genetics with marine ecology could provide a sensitive means of assessing evolutionary responses to climate change.

THE PHYSIOLOGICAL BASIS OF NATURAL SELECTION AT THE LAP LOCUS

An extensive research program was undertaken to evaluate the contribution of genetic variation at the Lap locus to variation in physiological traits under natural conditions. Rates of carbon and nitrogen metabolism were monitored in a population of the mussel Mytilus edulis near the center of the Lap allele frequency cline on the north shore of Long Island. The goal of this research was to establish whether the previously described genotype‐dependent differences in physiological phenotype are meaningful in ecologically relevant circumstances. It was predicted from laboratory studies that, in nature, genotype‐dependent differences will exist for rates of nitrogen excretion and that other aspects of the animals physiology, particularly rates of carbon metabolism, will be unaffected by Lap genotype.

Population genetics of marine species: the interaction of natural selection and historically differentiated populations

Abstract High gene flow, particularly as mediated by larval dispersal, has usually been viewed as sufficient to limit geographic isolation as a major source of population differentiation among marine species. Despite the general observation of relatively little geographic variation among populations of high dispersal marine species many cases of divergence have been observed and natural selection has usually been invoked to explain geographic divergence. Detailed study of several allozyme polymorphisms provided additional evidence that selection may be the predominant force that determines genetic divergence in marine systems. There is, however, growing evidence that marine species with high dispersal are more subdivided than originally thought. The use of multi-locus approaches and the application of molecular techniques have provided new insight into the nature of population divergence in marine species. I argue that (1) many species, which were formerly thought to be unstructured, are in fact subdivided into genetically discrete groups, (2) it is often the case that genetically subdivided populations have distinct evolutionary histories, (3) in many cases, natural selection is the consequence of introgression between these groups, and (4) the combination of molecular assays of both nuclear and mitochondrial DNA and allozyme loci provides the best approach to understanding the evolutionary dynamics of these interacting populations.

Growth trajectories of shell and soft tissue in bivalves: Seasonal variation in Mytilus edulis L.

Abstract A commonly used method for examining productivity in marine bivalves and other species with skeletal structures is to employ regression statistics to adjust dry tissue weights to an individual of standard size (usually length). Temporal variation in adjusted weights are then taken to reflect changes in productivity, fecundity or condition. This procedure assumes that changes in the covariate (length) are trivial. Here I describe a method that utilizes the presence of growth checks to determine separately rates of shell and soft tissue growth in the mussel Mytilus edulis L. The results indicate that rates of growth in shell and soft tissue do not occur simultaneously; in this case shell growth precedes the growth of soft tissue. Uncoupled patterns of growth seriously affect the results obtained using tissue weights adjusted to a standard length. Seasonal variation in adjusted weight provided no indication of true levels of productivity.

ASYMMETRIC INTROGRESSION OF MITOCHONDRIAL DNA AMONG EUROPEAN POPULATIONS OF BLUE MUSSELS (MYTILUS SPP.)

Abstract.—Mytilus edulis and M. galloprovincialis are two blue mussel species that coexist in western Europe. Previously, we reported that M. galloprovincialis populations contain female and male haplotypes that are fixed in M. edulis populations as well as unique haplotypes. This study assesses whether paraphyly for these species is due to introgression or incomplete lineage extinction. The lineage extinction hypothesis predicts that the shared mtDNA haplotypes in M. galloprovincialis will be significantly diverged from those in M. edulis and form distinct sequence clades. In contrast, the introgression hypothesis proposes that M. edulis haplotypes have only recently been introduced into M. galloprovincialis through hybridization with relatively little divergence accumulating between the shared RFLP haplotypes. We examined 80 mtl6S gene sequences for both the maternal and paternal mtDNA lineages from mussels sampled from various European populations and found strong support for the introgression hypothesis. In addition, we found that M. edulis mtDNA haplotypes appear to be introgressing into mussel populations in the Baltic Sea, which have predominantly M. trossulus nuclear genotypes, indicating that introgressive hybridization is prevalent among European mussel populations.

Trans-Pacific Range Extension by Rafting Is Inferred for the Flat Oyster Ostrea chilensis

Stretches of deep ocean are potent barriers to the dispersion of nearshore, benthic marine taxa. Such obstacles can be overcome, however, by species that have either a protracted pelagic larval development or a benthic life-history stage that can be transported by rafting (1, 2). The oyster Ostrea chilensis lacks an extended pelagic larval phase and has discrete populations in New Zealand and Chile that are separated by one of the largest extents (>7000 km) of open ocean on the planet. We tested competing dispersal hypotheses for this species by using ontogenetically informative, dated fossil and sub-fossil shell material, as well as molecular phylogenetic analyses. Our data show that dispersal by rafting is by far the most likely explanation for trans-Pacific range extension by this oyster, and we reject competing hypotheses of vicariance, anthropogenic introduction, and dispersal by ancestral lineages with extended larval development. The presence of 0. chilensis in Chile is important because it clearly demonstrates that transoceanic range extension by rafting is potentially available to a significant fraction of nearshore marine biotas.

Climate change, species distribution models, and physiological performance metrics: predicting when biogeographic models are likely to fail

Modeling the biogeographic consequences of climate change requires confidence in model predictions under novel conditions. However, models often fail when extended to new locales, and such instances have been used as evidence of a change in physiological tolerance, that is, a fundamental niche shift. We explore an alternative explanation and propose a method for predicting the likelihood of failure based on physiological performance curves and environmental variance in the original and new environments. We define the transient event margin (TEM) as the gap between energetic performance failure, defined as CTmax, and the upper lethal limit, defined as LTmax. If TEM is large relative to environmental fluctuations, models will likely fail in new locales. If TEM is small relative to environmental fluctuations, models are likely to be robust for new locales, even when mechanism is unknown. Using temperature, we predict when biogeographic models are likely to fail and illustrate this with a case study. We suggest that failure is predictable from an understanding of how climate drives nonlethal physiological responses, but for many species such data have not been collected. Successful biogeographic forecasting thus depends on understanding when the mechanisms limiting distribution of a species will differ among geographic regions, or at different times, resulting in realized niche shifts. TEM allows prediction of the likelihood of such model failure.