Dr. Matthew P. Hare
Assistant Professor

Department of Biology
University of Maryland
College Park, MD 20742

email: matthare@umd.edu
office phone: (301) 405-7264
lab phone: (301) 405-7260
fax: (301) 314-9358

Matt’s research goals are to understand the ecological, demographic and historical processes that generate population substructure and species diversity in coastal marine ecosystems, and to make these findings relevant to conservation and management when possible. In marine environments there are few absolute barriers to dispersal, yet population genetic substructure and cryptic species are common in marine taxa that have high dispersal potential. This implicates cryptic barriers to dispersal or strong diversifying selection generating population substructure. Matt’s work focuses on both these possibilities by using genetic markers to test for larval retention and nonrandom dispersal limiting population admixture, and by testing for the effects of natural selection at both genetic and phenotypic levels. Conventional means of studying these population processes are made difficult in the diverse taxa studied in the Hare lab because of their small size (invertebrate larvae, copepods), phenotypic plasticity of adults, or parasitic life cycles. By analyzing genetic variation using phylogenetic, population genetic and biogeographic frameworks, Matt’s research overcomes some of these obstacles and infers population processes affecting spatial connectivity at both ecological and evolutionary time scales.

Postdocs
            Inken Kruse

Technician
            Katie Shulzitski

Graduate Students
            Colin Rose
            Gang Chen
            Maria Murray
            Peter Thompson
            Safra Altman (co-advised with Tuck Hines)
            Sarah Kingston (co-advised with Mike Braun)
            Andreanna Welch (co-advised with Rob Fleischer)

Undergraduates
            Kristina Cammen
            Andrew Ascione
            Ying Yi Zheng
            Emmanuel Mallam

Current Research Topics

Diversification at a zoogeographic province boundary

Clustered species range limits in eastern Florida form a widely recognized boundary between warm-temperate and sub-tropical faunistic provinces. A compression of latitudinal thermoclines along the Florida coast implicates climate as a driving force shaping this community transition, but few studies have directly compared the importance of climate versus hydrographic dispersal barriers or species interactions. The eastern oyster, Crassostrea virginica, is nearly-continuously distributed around Florida, providing an exceptional intraspecific model for distinguishing the relative importance of pre- and postsettlement mechanisms structuring estuarine populations across the province boundary in eastern Florida. A major goal in the Hare lab is to understand the biotic and abiotic factors that maintain population differentiation in the oyster, and then test the generality of these influences on other codistributed species.

The oyster cline has had a stable ‘stepped’ shape centered at Cape Canaveral for the past dozen years (~6 generations; Murray and Hare submitted). Both dispersal barriers and selection could be maintaining the cline. Oysters only occur in the hydrographically semi-closed lagoons behind barrier beaches in eastern Florida, where larval dispersal is predicted to be small-scale, bidirectional and follow a stepping-stone pattern. However, if larvae are flushed out and re-enter lagoons, then coastal currents may generate a leap-frog and directional pattern of dispersal. Dispersal directionality could be a particularly important aspect of this system, and province boundaries in general, because asymmetrical gene flow can steepen clinal variation and truncate species ranges along a selection gradient (Hare et al. 2005). Multilocus assignment tests on newly-settled oysters are being used to measure dispersal distances and direction without recourse to equilibrium theory and to test for patterns predicted from known dispersal constraints and current flow patterns.

The spatial scale of population structure is determined by a balance between dispersal-mediated connectivity and spatially variable selection. Along the eastern Florida ecotone, oyster dispersal patterns are being interpreted in combination with the spatial pattern and magnitude of selection as measured by postsettlement cohort analyses and reciprocal transplants. Maria Murray’s Ph.D. research goals are to distinguish three models by which selection may maintain the oyster cline, (1) hybrid unfitness relative to parentals regardless of habitat, (2) habitat-specific hybrid unfitness, and (3) bounded hybrid superiority, with hybrid success constrained to intermediate habitats. She is measuring fitness-related traits including growth rate, survivorship, size-corrected fecundity, thermal tolerance and parasite load.

At present, the strongest evidence for divergent selection across the oyster cline comes from a genomic screen of AFLP loci in which locus-specific Fst estimates were used to calculate a genomic mean Fst. A null distribution of Fst was then simulated under neutral drift given the empirical mean Fst (Murray and Hare submitted). Nonequilibrium and equilibrium simulations were compared to show that the expected neutral variance in Fst, for a given genomic mean, is unaffected by secondary contact history. In a comparison of one population each from the Atlantic and Gulf of Mexico (representing the two tails of the eastern Florida oyster cline), 2-7% of polymorphic AFLP loci had Fst estimates outside the simulated 99th quantile for Fst. A similar test applied to previously-published codominant oyster loci identified only one non-neutral locus (3.7%). Thus, our genomic screen using AFLPs indicates that a small portion of the genome is shaped by divergent selection. Candidate non-neutral loci will be converted to codominant markers, mapped onto an existing C. virginica genetic map, and used to resolve the genetic basis for relative fitness differences.

Diversification along salinity gradients

Acartia tonsa is a seasonally dominant species of estuarine copepod along the eastern U.S. coast. Enormous populations of this species graze phytoplankton in the water column and provide an important prey item for fish. As with all zooplankton with a high potential for long-distance dispersal mediated by hydrographic currents, allopatric differentiation is only expected at the largest of geographic scales. We have found several deeply divergent mitochondrial DNA lineages within A. tonsa sampled from Chesapeake Bay. While deep mitochondrial lineages were previously reported within A. tonsa, Gang Chen has shown that they represent cryptic, reproductively isolated species based on genealogical concordance across mitochondrial and nuclear loci (Chen and Hare in prep.). Cryptic species are not novel or surprising in marine invertebrates any more, but in this case ecological speciation is suggested by their parapatric distribution along salinity gradients—one lineage is only found at salinities below 11 ppt, while another only occurs above that threshold. This habitat specificity could result from speciation in situ along salinity gradients, with each tributary containing sister species of high- and low-salinity copepods. Alternatively, a low-salinity clade might be relatively ancient, with representative populations now occupying most low-salinity habitat patches via colonization. Preliminary phylogeographic results support the latter hypothesis and suggest that the more discontinuous habitat used by the low salinity lineage has promoted allopatric speciation at spatial scales over which the high salinity lineage is only modestly subdivided. Thus, among estuarine species, the apparent propensity for dispersal is far less informative about allopatric diversification than the discreteness of habitat patches. We will be comparing the phylogeography of each A. tonsa lineage to define the geographic scale at which gene flow is constrained. Direct testing of relative fitness at different salinities is also planned to determine the relative importance of selection enforcing population structure across salinity gradients versus gene flow differences among lineages being a simple function of dispersal constraints among habitat patches.

Conservation Genetics - Invasive Marine Parasites

Macro- and microparasites in marine systems can have strong effects on community structure and devastating consequences for fisheries. Genetic markers are an under-utilized tool for more thoroughly describing parasite diversity, inferring population structure, and tracing the circumstances that promote changes in geographic range or host spectrum. Work in the Hare lab is focused on these goals with two highly-virulent parasites. Eastern oysters suffer severe mortality from epidemic infections by the protist Perkinsus marinus. This parasite was originally known from the Gulf of Mexico north to Chesapeake Bay, but infections have now become common and severe in New England due to an apparent range expansion. The P. marinus genome is being sequenced as a representative of basal apicomplexans, yet very little is known about its population structure and the relative importance of clonal versus sexual reproduction. Almost all information on this species derives from clonal laboratory cultures. In the Hare lab we use a more direct approach to assay genetic variation in wild strains by using species-specific primers to PCR amplify P. marinus DNA from genomic DNA of infected oysters. We have found evidence for abundant sexual recombination within a local population (Hare and Thompson in prep.). Peter Thompson is testing the generality of this result across the range of P. marinus, describing phylogeographic structure at neutral and candidate virulence-related loci, and reconstructing the demographic pattern of range expansion. Our genetic description of population processes and population history will inform efforts to manage the devastating effects of this parasite on oyster fisheries.

Research efforts in the Hare lab are also focused on tracing the invasion history of a rhizocephalan (barnacle) parasite that castrates estuarine mud crabs. Loxothylacus panopaei is endemic to the Gulf of Mexico and southeastern Florida, but was introduced to Chesapeake Bay in 1964. Inken Kruse, currently a postdoc at the Smithsonian Marine Station in Fort Pierce, FL, has found that the invasive Chesapeake population is (1) genetically quite distinct from endemic populations in southeastern Florida, (2) infects a different spectrum of broadly-distributed mud crab species than in the endemic range, and (3) is expanding its range southward into Florida such that contact with the endemic population is expected in the next few years (Kruse and Hare in prep.). We are developing molecular assays to detect early stages of crab infection and Inken is experimentally testing the ability of different parasite populations to infect the same broadly distributed host species. Results of these studies will help determine the source population for the Chesapeake invasion, help clarify why this invasion has been successful, and may help determine why a congeneric rhizocephalan parasite infects only southern populations of its commercially valuable host, blue crab.

Conservation Genetics – Eastern Oysters in Chesapeake Bay

The goal of our research on C. virginica in Chesapeake Bay is to test the effectiveness of current restoration efforts and facilitate those efforts by estimating the scale of larval dispersal. This work is collaborative with the Virginia Institute of Marine Science and funded through the NOAA/SeaGrant national Oyster Disease Research Program. Because restoration strategies increasingly include the planting of selectively-bred disease tolerant C. virginica broodstock, an additional goal of our research is to evaluate the genetic health of Chesapeake oyster populations and the impact of introgression from restoration plantings.

Using microsatellites to test for temporal and spatial subdivision within Chesapeake Bay, Colin Rose found no evidence for temporal heterogeneity and subtle spatial differentiation consistent with isolation by distance (IBD). This IBD pattern could be an evolutionary equilibrium emerging from stepping-stone dispersal. Alternatively, anthropogenic activities related to fisheries management and restoration may be creating or eroding an IBD pattern. An evolutionary interpretation seems more parsimonious for several reasons (Rose et al. in press), but more work is needed to distinguish these potential mechanisms and strengthen our conclusion that oyster recruitment is primarily within tributaries or between adjacent tributaries. One such effort includes our direct estimates of oyster dispersal distances based on genetic tags. The ‘tagging’ is a consequence of genetic drift and selection during breeding of C. virginica for disease tolerance, and further bottlenecks imposed during each hatchery spawn of selected-strain broodstock needed to produce juveniles for restoration plantings (Rose and Hare in prep.). In a tributary where tagged oysters were planted on a single reef, we have traced dispersal of their progeny by using assignment tests on the multilocus genotypes of newly-settled juveniles collected throughout the tributary. In the year with the highest overall recruitment thus far, almost 1600 oyster juveniles were collected and genotyped for eight microsatellite loci and mitochondrial DNA. We estimated that during that year 9.7% of juveniles originated from parents at the point source (Hare et al. in press). Sampling is not yet sufficient to characterize average dispersal distances, but this overall level of population enhancement was much lower than anticipated, precipitating critical evaluation of untested assumptions underlying restoration methods.

Conservation Genetics – Genetic Diversity of Endangered Marine Mammals

One of the risks faced by severely depleted species is the loss of reproductive fitness potentially incurred through inbreeding. The severity of inbreeding depression in a small remnant population depends, in part, on the history of inbreeding experienced by the species. Using recently developed population genetic theory focusing on patterns of variation across loci in the genome rather than across individuals in the population, extant genetic variation can provide estimates of genetic diversity that existed in ancestral populations. These methods offer an approximate means to compare the relative levels of inbreeding through time in terms of effective population size. Nuclear intron sequences were collected from two marine mammal species that experienced severe population size reductions and now have relatively low genetic diversity; North Atlantic right whales and northern elephant seals. The strong recovery of healthy elephant seal populations after legal protection suggests low vulnerability to severe inbreeding depression, whereas right whales remain critically endangered after six decades of protection. The patterns of variation across introns at fourteen independent loci have reaffirmed and strengthened the identification of a new right whale species (Hare and Palumbi 2003; Gaines et al. 2005) and are consistent with relatively large effective population sizes in the ancestry of both elephant seals and right whales (Hare in prep.). Low genetic diversity seems to be a recent trend in both these lineages, not an ancestral characteristic.

Representative Publications

Hare, M. P., S. K. Allen Jr., P. Bloomer, M. D. Camara, M. D. Carnegie, J. Murfree, M. W. Luckenbach, D. Merritt, C. Morrison, K. T. Paynter, K. S. Reece, and C. G. Rose. 2006. A genetic test for recruitment enhancement in Chesapeake Bay oysters, Crassostrea virginica, after population supplementation with a disease tolerant strain. Conservation Genetics Online First, DOI: 10.1007/s10592-005-9108-3.

Rose, C. G., K. T. Paynter, and M. Hare. 2006. Isolation by distance in the eastern oyster, Crassostrea virginica, in Chesapeake Bay. J. Heredity 97(2):158-170.

Hare, M.P., C. Guenther and W.F. Fagan. 2005. Nonrandom larval dispersal can steepen marine clines. Evolution 59:2509-2517.

Gaines, C.A., M.P. Hare, S.E. Beck and H.C. Rosenbaum. 2005. Nuclear markers confirm taxonomic status and relationships among highly endangered and closely related right whale species. Proceedings of the Royal Society B 272:533-542.

Hare, M.P. and J. Weinberg. 2005. Phylogeography of surf clams, Spisula solidissima, in the western North Atlantic based on mitochondrial and nuclear DNA sequences. Marine Biology 146:707-716.

Robinson T.B., C.L. Griffiths, A. Tonin, P. Bloomer & M.P. Hare. 2005. Naturalized populations of Crassostrea gigas along the South African coast: distribution, abundance and population structure. Journal of Shellfish Research 24(2):443-450.

Hare, M.P. and S.R. Palumbi. 2003. High intron sequence conservation across three mammalian orders suggests functional constraints. Molecular Biology and Evolution 20(6): 969-978.

Hare, M.P., F. Cipriano and S.R. Palumbi. 2002. Genetic evidence on the demography of speciation in allopatric dolphin species. Evolution 56:804-816.

Hare, M.P. 2001. Prospects for nuclear gene phylogeography. Trends in Ecology and Evolution 16(12):700-706.

Palumbi, S. R., F. Cipriano and M. P. Hare. 2001. Predicting nuclear gene coalescence from mitochondrial data: The three-times rule. Evolution 55:859-868.

Hare, M.P., S.R. Palumbi and C.A. Butman. 2000. Single-step species identification of bivalve larvae using multiplex polymerase chain reaction. Marine Biology 137:953-961.

Hare, M.P. and S. R. Palumbi. 1999. The accuracy of heterozygous base calling from diploid sequence and resolution of haplotypes using allele-specific sequencing. Molecular Ecology 8:1750-1752.

Hare, M.P. 1998. Using mitochondrial DNA gene trees and nuclear RFLPs to predict genealogical patterns at nuclear loci: examples from the American oyster. Proceedings of the trinational workshop on molecular evolution, M. Uyenoyama and A. von Haeseler, eds. Duke Publications Group, Duke University, Durham, NC.

Hare, M.P. and J.C. Avise. 1998. Population structure in the American oyster as inferred by nuclear gene genealogies. Molecular Biology and Evolution 15:119-128.

Orti, G., M.P. Hare, and J.C. Avise. 1997. Detection and isolation of nuclear haplotypes by PCR-SSCP. Molecular Ecology 6:575-580.

Hare, M.P. and J.C. Avise. 1996. Molecular genetic analysis of a stepped multilocus cline in the American oyster (Crassostrea virginica). Evolution 50:2305-2315.