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Our lab group strives to do question based, hypothesis driven research that advances our understanding of ecological and evolutionary processes in marine environments. We work on a diverse taxonomic groups ranging from fish to molluscs to crustaceans to bacteria. Although lab members are engaged in a wide variety of independent research projects, most of the work in the lab is organized around three themes:

1) Dispersal and connectivity in marine environments
2) The evolution of marine biodiversity

3) Dispersal and Ecological Adaptation in Marine Environments

4) Marine conservation

Dispersal and connectivity in marine environments
    Although most people envision wide-ranging, highly mobile species like tuna or whales when thinking of marine organisms, the vast majority of marine species are sedentary or have limited mobility as adults. Even reef fish that are very mobile are typically restricted to single coral reefs or even small sections of a given reef. Rather than dispersing as adults, most marine organisms have a dispersive larval developmental phase that can last from a few hours to many months. Although some larvae have very limited dispersal capabilities, others spend extended periods of time in the water column where theory suggests they can be dispersed vast distances on ocean currents. Local populations are thus sustained by the recruitment of larvae from distance sources a process referred to as connectivity. However, research on larval dispersal and connectivity has been hampered by the fact that marine larval can be very very small and the oceans are vast, making direct observation of potentially highly dispersive larvae difficult or impossible. Understanding the process of dispersal and demographic connectivity in marine environments is crucial both for the understanding the factors that influence the dynamics of marine populations as well as developing effective management strategies that ensure sustainable marine resources and the preservation of marine biodiversity.
    In recent years, molecular genetics has contributed significantly to understanding larval dispersal and connectivity because dispersal patterns can be inferred by comparing patterns of genetic similarity among populations. Although some species exhibit genetic uniformity over broad geographic ranges as predicted, other species show strong genetic differentiation among populations from different geographic regions, indicating that larval dispersal can be more limited than we believe. These genetic studies have been complimented by innovative methods where larvae are marked using natural or artificial chemical signatures so that the geographic origins or larval recruits can be determined. Such studies have demonstrated that many fish larvae, despite the ability to disperse, actually recruit back to their natal reefs.
    We have an active research program focused on the application of molecular genetic techniques to understanding larval dispersal and connectivity in marine environments. Although we work in a number of regions of the world, most of our work is focused on the waters of Indonesia, a region with a pronounced physical oceanography (Fig. 1). To date, most of our work has focused on stomatopods and has shown that contrary to predictions, the strong currents of the Indonesian Throughflow do not result in connectivity between Northern and Southern Indonesian populations of the stomatopod Haptosquilla pulchella (Fig. 2) (Barber et al. 2000, 2002). However, predictions of limited connectivity across the Malucca Sea based on limited water transport resulting from the Halmahera Eddy (Fig. 1) are supported by genetic analysis (2002). These results have been corroborated with comparisons in other stomatopod taxa (Barber et al. in prep.).

Through an NSF CAREER grant and PIRE grant, we are now actively testing how the physical environment of the Coral Triangle interfaces in the ecology and life-histories of adults and larvae of a wide variety of marine vertebrate and invertebrate species to shape patterns of connectivity in the Indo-West Pacific. In particular, the PIRE project will be integrating multi-locus genetic measures of connectivity with predictive geospatial models of connectivity, created by Eric Treml. Through these efforts we hope to better understand the origins of marine biodiversity in the Coral Triangle as well as help guide managers as they endeavor to develop effective networks of MPAs throughout this region.

Fig. 1. The physical oceanography of the Indo-West Pacific. Indonesian Throughflow originates in North Equatorial Current (NEC) of the Pacific and passes through the waters of Indonesia before joining the South Equatorial Current (SEC) of the Indian Ocean. The New Guinea Coast Current (NGCC) is retroflected by the Halmahera Eddy (HE), limited water transport across the Malucca Sea (Mal. Sea) . High water transport (20 million cubic meters of water per second) of the Indonesian Throughflow is predicted to facilitate connectivity, while the Halmahera Eddy is predicted to limit connectivity by limiting east to west water movement across the Malucca Sea.
Fig. 2. The genetic composition of Haptosquilla pulchella populations through out the Indo-West Pacific. Diagram in the upper right depicts the relationship of unique DNA sequences of the mitochondrial cytochrome oxidase-1 gene. Individual groups are color coded. Pie diagrams on map indicate the relative frequency of each of these color coded groups. Notice that the light blue group is separated by a large genetic break (34 mutations) from population to the west of the Malucca Sea. The white group only occurs in southern Indonesia and is separated by a large genetic break (36 mutations) from populations north of the Flores Sea. Even within Indonesia, the distribution of red, orange, green, gray, yellow, and blue groups indicates regional genetic differentiation, indicating that larval dispersal is less than predicted.

 

The evolution of marine biodiversity
The Indo-West Pacific is the center of the world's marine biodiversity, yet explanations for this high diversity are lacking. It is often suggested that this region is a Center of Origin- that is, speciation occurs within this region, then biodiversity is exported to peripheral populations in the Pacific and Indian Oceans. However, this theory requires a mechanism for driving speciation within the center of diversity.
    The traditional allopatric model of speciation applied in terrestrial ecosystems often seems inadequate to explain high
diversity in marine ecosystems as most marine organisms have pelagic larval stages that should limit the opportunities for geographic and reproductive isolation, and there are few clear barriers to dispersal in the sea. However, our work in connectivity of stomatopods in Indonesia has suggested that ecology and physical oceanography may play a role in limiting larval dispersal, leading to allopatric speciation. Funded by a National Science Foundation CAREER grant we will integrate ecology, physical oceanography, and molecular genetic techniques to explore the evolution of marine biodiversity in the Indo-Pacific. Our work is focused on two biogeographic regions. The first, the Halmahera Eddy (Fig. 1) limits water transport from the New Guinea into Indonesia. As water transport is limited, larval transport should be similarly limited. We are comparing patterns of genetic differentiation across the biogeographic boundary in a variety of species that have long/short, active/passive larval periods, as well as species that are sedentary or mobile as adults. By comparing genetic patterns in mitochondrial and nuclear genes across a ecologically diverse group of species, we hope to determine whether the Halmahera Eddy is a dispersal barrier capable of promoting speciation in this region. Similarly, we we compare patterns across the Flores Sea. The Flores Sea is spanned by hundreds of small, oceanic low coral islands. Although many coastal species can inhabit these regions as well, there are species that are ecologically excluded from these "stepping-stones". We are comparing patterns of genetic differentiation across this region in a variety of marine species that can and cannot utilize these habitats in hopes of determining whether certain ecologies may promote speciation because these ecologies limit access to "stepping-stones", limiting dispersal and promoting speciation.

Dispersal and Ecological Adaptation in Marine Environments
   
Although vicariance is considered the dominant mode of lineage diversification, differential selective pressures can also create regional genetic variation and/or species diversity. However, this mode of speciation is believed to be rare in marine organisms, partially due to the perceived homogeneity of the marine environment, but primarily to the belief that the vagility of marine organisms, either as adults or larvae, would result in gene flow swamping out regional selection, limiting local adaptation.

In this collaborative NSF funded project, David Conover and I are addressing the paradox of local adaptation in a regime of potentially high gene flow in Menidia menidia . We have embarked on a fine-scaled analysis of regional phenotypic and genetic diversification in Atlantic silversides along a latitudinal gradient to determine the degree to which phenotype and genetic diversity are co-vary across latitude and may therefore be a function of limited dispersal or selection pressures along the coast. In particular, we will be focusing on potential environmental/dispersal discontinuities at biogeographic barriers such as Cape Cod and Cape Hatteras that could indicate a linkage between limited genetic exchange among populations and phenotypic ecologically driven diversification. However, it is possible that no correlation between phenotypic variation and molecular genetic variation will be observed. This remarkable result would indicate that adaptive phenotypic variation can evolve independently of historic patterns of gene flow, and would suggest that strong selection could result in the creation of biodiversity without the detectable physical or genetic isolation of populations.

      In addition to this NSF funded project, I am completing a collaborative project with Peter Doherty, Mark Meekan, and Laurent Vigliola to examine the evolutionary consequences of size-selective mortality that occurs during the process of recruitment of larval fish onto coral reefs. In this project we have shown a pronounced correlation between ecological selection and the genetic composition of a cohort of larval fish at a mitochondrial gene , whereas microsatellite data show no significant response to selection. As ecological selection favors the survivorship of fast growing fish, and growth rate is a function of mitochondrial performance, an intriguing link exists between the ecological process of predation, physiological performance, and the genetic evolution of the population. In particular, analysis of secondary structure of the mtDNA control region indicates that size and growth rate are correlated with the number and availability of VNTR regions containing Termination Associated Sequences, available for regulation of replication.


Marine Conservation
   
Although much of our work is designed to improve our understanding of basic ecological and evolutionary processes in marine environments, the results have strong conservation implications. We are active in interfacing with conservation organizations and resource managers such as Conservartion International and The Nature Conservancy so that our primary research can be translated into improved marine resource management. Long-term persistence of local marine populations may depend upon larval import from distant coral reefs, and determining patterns of connectivity in marine environments will facilitate the siting and spacing of marine reserves so that connectivity is preserved. The discovery of pronounced regional genetic differentiation indicating the lack of genetic connectivity may indicate dispersal barriers that limit demographic exchange among geographic regions or the presence of cryptic biodiversity. This data in turn can help define consrvation prioritregional management units.
    In 2005 we were funded by Conservation International to directly incorporate genetic data into the formation of conservation policy within the Coral Triangle as part of a collaborative effort between the Indonesian Government, Conservation International, The Nature Conservancy, and World Wildlife Fund. In this project, we are examining patterns of genetic connectivity on fine geographic sacles within the Raja Ampat region of Eastern Indonesia in a variety of reef functional groups from reef builders to pelagic predators. By comparing levels of connectivity within this seacape between this and other seascapes in the Coral Triangle we can evaluate the degree to which biogeographic regions in the Coral Triangle may be demographically independent and in need of regionally focused management plans. This data will then be integrated with a variety of ecological, social, and political data to form a more comprehensive management plan for one of the world's most diverse and threatened ecosystems.