Overview of Research Interests: The Blakeslee lab focuses on conservation biology in marine systems and includes a diverse research program involving biodiversity, population genetics, parasite ecology, and biogeography—as well as the unique and integrative insight that can be gained from studying biological invasions. Recently, biological invasions have become recognized as a major contributor to the global (and often disjunct) distributions of many marine species as a result of human transport mechanisms. Invasion research is therefore important not only from a conservation perspective but can provide theoretical and practical understanding of population and community level influences of novel species, and can also serve as an important teaching tool for students and the general public. Marine invasions are a major part of human-induced global change, including population, community, and ecosystem-level shifts in marine biota, genetics, and the environment. We examine many integrative aspects of marine invasions, focusing in four major areas: (1) global distribution patterns and biogeography of free-living and parasite species, (2) marine invasions and vectors, (3) population genetics and population ecology in native and non-native populations, and (4) community ecology and host-parasite interactions of native and non-native organisms, including host behavior, physiology, and genetics. We focus our studies primarily on marine invertebrates as they have contributed vast numbers of introductions globally, and they also serve as hosts to marine parasites, which are a fundamental but often overlooked component of many marine systems, and which can become cryptic invaders themselves.
(1) Global Distribution Patterns and Biogeography: Due to centuries of human-mediated dispersal superimposed upon millions of years of natural dispersal, many organisms have complex biogeographic patterns. Species may clearly occupy natural ranges, be introduced to new regions, or have ambiguous (cryptogenic) histories. Distinguishing among them can be challenging, requiring multiple lines of evidence. My research has employed genetics, demographics, and parasites as tools to better understand biogeographic and phylogeographic patterns of species with natural, ambiguous, or non-native ecological histories. For my doctoral research, I used genetic and parasite signatures to settle the 100-yr debate over the native/non-native status of N. American Littorina littorea (common periwinkle), a highly abundant and influential snail. My work also contributed a novel approach for the resolution of its cryptogenic status. Using signatures of parasite escape in trematodes and congruent patterns in host and parasite molecular data, we found a significant reduction in parasite diversity compared to native congeners, as well as apparent founder effect signatures in L. littorea and its most common parasite. An additional study combining historical shipping records with molecular data also found corroborative evidence that L. littorea and an algal species were likely introduced with solid ballast from timber-carrying ships from the British Isles (particularly Ireland and Scotland) in the 1700-1800s.Thus, using multiple lines of evidence, we were able to conclude that N. American L. littorea is an introduced species from Europe (Blakeslee & Byers 2008, Ecology; Blakeslee et al. 2008, Mol. Ecol.; Brawley et al. 2009). L. littorea is also found in several unquestionably non-native populations on the US west coast, but the source and vector of introduction had been unclear. We collected demographic and molecular data from the west coast, revealing curious signatures of a pre-establishment phase of introduction (i.e., uniform size-frequencies of adults and no genetic bottleneck). This suggested that the snail was being repeatedly and intentionally introduced (probably from Asian markets) but had not yet established sustainable populations in the region (Chang et al. 2011).
I have also investigated biogeographic and phylogeographic patterns in the rough periwinkle snail, Littorina saxatilis—a model species for evolutionary studies of speciation due to its reproductive strategy of brooding crawl-away young. Until recently, its phylogeography in the N. Atlantic was unknown. In a collaborative study with Kerstin Johannesson’s lab (Goteborg Univ, Sweden), we uncovered long-term separation (prior to the last glaciation) between Atlantic coasts and a clear stepping-stone migration across N. Atlantic islands (Panova et al., 2011). L. saxatilis is also interesting because of its broad physiological tolerances and ability to survive in numerous coastal habitats; this along with its direct developing reproductive mode has resulted in the evolution of locally-adapted phenotypes (‘ecotypes’). To date, little is known about ecotypes in North America; thus my graduate students and I have been examining them across a broad biogeographic range (Nova Scotia to Long Island), collecting morphological, reproductive, habitat, parasite, and genetic data. Aspects of this work are part of the master’s thesis of two prior graduate students at LIU-Post (Leidy Leon and Martha Sanderson) and so far, we have found significant differences among ecotypes across all levels of investigation. We have also collected mitochondrial sequences from multiple populations in the region, and in the near future, I will obtain microsatellite data and genomic data to look for ecotypic differentiation across these different populations.
I have also investigated biogeographic and phylogeographic patterns in the rough periwinkle snail, Littorina saxatilis—a model species for evolutionary studies of speciation due to its reproductive strategy of brooding crawl-away young. Until recently, its phylogeography in the N. Atlantic was unknown. In a collaborative study with Kerstin Johannesson’s lab (Goteborg Univ, Sweden), we uncovered long-term separation (prior to the last glaciation) between Atlantic coasts and a clear stepping-stone migration across N. Atlantic islands (Panova et al., 2011). L. saxatilis is also interesting because of its broad physiological tolerances and ability to survive in numerous coastal habitats; this along with its direct developing reproductive mode has resulted in the evolution of locally-adapted phenotypes (‘ecotypes’). To date, little is known about ecotypes in North America; thus my graduate students and I have been examining them across a broad biogeographic range (Nova Scotia to Long Island), collecting morphological, reproductive, habitat, parasite, and genetic data. Aspects of this work are part of the master’s thesis of two prior graduate students at LIU-Post (Leidy Leon and Martha Sanderson) and so far, we have found significant differences among ecotypes across all levels of investigation. We have also collected mitochondrial sequences from multiple populations in the region, and in the near future, I will obtain microsatellite data and genomic data to look for ecotypic differentiation across these different populations.
(2) Marine Invasions and Vectors: Not only have I investigated marine invasions from a biogeographic perspective, but I am also interested in understanding it from the population and community-level perspectives, as well as better understanding the marine introduction vectors that transport organisms from place to place. Below I describe some of my recent work in these areas. While in Long Island, I collaborated with colleagues on the distributions and population demographics (abundance, sex ratios, size-frequency distributions) of native panopeid mud crabs and the invasive Asian shorecrab (Hemigrapsus sanguineus). We found significant negative correlations between the crabs; i.e., native mud crabs densities negatively correlated with H. sanguineus densities. We also explored the distribution and spread of a newly-invasive castrating rhizocephalan barnacle (Loxothylacus panopaei) that likely invaded from non-native Mid-Atlantic populations (Freeman, Blakeslee et al., 2013, Aquatic Invasions). This parasite infects native mud crabs but not H. sanguineus. We surveyed multiple Long Island populations to determine whether L. panopaei’s invasion could have community-wide impacts, given its strong reproductive effect on these ecologically important mud crabs. Altogether, we documented further spread of the parasite to several new Long Island populations. In addition, a high school student (I. Kernin) and I explored survival rates in infected and uninfected mud crabs interacting with H. sanguineus, finding that infected mud crabs were preyed upon by H. sanguineus at a faster rate than uninfected mud crabs. This lab exploration was further supported by a similar study in a local field site at Cold Spring Harbor labs, which was highlighted in their web-blog in June 2015 (http://labdish.cshl.edu/2015/06/23/lending-a-shore-to-fellow-li-researchers/). All this research is being analyzed for future publication. Additionally, a former LIU-Post honors student in my lab (Kelley Kroft) explored parasite diversity in H. sanguineus and local mud crabs from numerous eastern U.S. populations (with a focus on Long Island) to determine if there were differences in parasite loads between the crab species, and if H. sanguineus continued to show strong parasite escape. She found greater parasite diversity in mud crabs versus H. sanguineus and also identified a new native parasite infecting H. sanguineus. Kelley's honors thesis was recently published (Kroft & Blakeslee 2016). While at LIU-Post, another graduate student’s work (Michael Roy) included a vast demographic and parasite survey of Long Island, exploring the recent invasion of an Asian grass shrimp, which heretofore had only been recorded in the Bronx River estuary and Mystic River. Michael’s study was the first to document the invasive shrimp in several previously unreported locations along the north and south shores of Long Island, providing important baseline information for non-native species at early stages of invasion. Michael also co-mentored a 2014 undergraduate summer intern (L. Moritzen) on a project she independently designed exploring significant factors influencing the densities of grass shrimp at several Long Island sites. Her research served as the basis for her honors thesis at Rider University, and we are presently working on a manuscript for publication.
Specific to marine introduction vectors, I was a co-PI for a MD SeaGrant award with colleagues at SERC. Our project explored an understudied vector, the live baitworm trade, which has led to the invasion and range expansion of several marine organisms (including C. maenas and L. saxatilis). This vector ships Maine baitworms with algal packing materials, which can contain hundreds of hitchhiking individuals. Our team studied the species diversity, functional diversity, and genetic diversity of the hitchhikers at all steps along the invasion pathway from distributor to baitshop (Fowler, Blakeslee, et al., 2015). Additionally, we performed applied experiments to determine inexpensive and easily implementable methodologies for reducing hitchhikers in the algae (Blakeslee et al., in press). Altogether, this highly collaborative project, involving ecologists, molecular biologists, and social scientists, allowed us to understand in detail a tractable introduction vector and determine ways in which to reduce impacts on marine communities.
Specific to marine introduction vectors, I was a co-PI for a MD SeaGrant award with colleagues at SERC. Our project explored an understudied vector, the live baitworm trade, which has led to the invasion and range expansion of several marine organisms (including C. maenas and L. saxatilis). This vector ships Maine baitworms with algal packing materials, which can contain hundreds of hitchhiking individuals. Our team studied the species diversity, functional diversity, and genetic diversity of the hitchhikers at all steps along the invasion pathway from distributor to baitshop (Fowler, Blakeslee, et al., 2015). Additionally, we performed applied experiments to determine inexpensive and easily implementable methodologies for reducing hitchhikers in the algae (Blakeslee et al., in press). Altogether, this highly collaborative project, involving ecologists, molecular biologists, and social scientists, allowed us to understand in detail a tractable introduction vector and determine ways in which to reduce impacts on marine communities.
(3) Population Genetics and Population Ecology: A global invader I have extensively researched over the past several years is the European green crab (C. maenas), which has had at least two introduction events (historical and recent) to eastern N. America from different European populations. Due to the prevailing southerly currents from Nova Scotia into the Gulf of Maine, the crab’s novel northern alleles have been mixing with alleles from the crab’s original introduction, resulting in allele frequency changes as the invasion front spreads southwards (Fig 1); however, there has not been complete replacement of the historical genotypes due to the presence of retention zones (Pringle, Blakeslee et al., 2011). This genetic admixture also allowed us to resolve the recent invasion of C. maenas to Newfoundland by using molecular methods (mtDNA and microsatellites), demographic data, and Canadian shipping records, in which we found Newfoundland populations to share similar allele frequencies with crabs from the central/western Scotian shelf (nearby Halifax). Thus, C. maenas overcame considerable physical, evolutionary, and ecological obstacles via anthropogenic transport to become established and abundant in Newfoundland (Blakeslee et al., 2010). A related project focuses on the nuclear vs. mitochondrial introgression of northern and southern genotypes in N. America, which appears to be much slower in nuclear vs. mitochondrial genes. We believe this may be related to the maternal inheritance of mitochondrial genes, as well as the ‘stickiness’ of the alleles in an occupied versus unoccupied front (Darling et al., 2014). In the future, we intend to continue exploring temporal changes in allele frequencies as the invasion front continues to progress southwards. In fact, I am currently collaborating on updating our current understanding of this dynamic invasion front, as well as the population admixture and its continued anthropogenic expansion, as well as exploring geometric morphometrics using samples collected for genetic analysis from 2013-2015.
I am also finalizing analyses on a host-parasite population genetics study in the eastern mudsnail, Ilyanassa obsoleta, introduced to the N. American west coast in the early 1900s, where it is infected by a subset of its native parasite diversity (Blakeslee et al., 2012, J. Biogeog.). My results demonstrate a differential effect of introduction on genetic diversity in the host snail compared to its parasites (Blakeslee et al., in prep), likely due to inherent differences in host-parasite life histories, vector propagule pressure, and survivorship, leading to greater genetic bottlenecks in the parasites. In the future, I would like to investigate other hosts, particularly west coast natives, because the addition of new parasites to the region is likely influencing community interactions. For example, the trematode Austrobilharzia variglandis has been implicated in outbreaks of swimmer’s itch in some west coast communities where I. obsoleta is invasive but is rarely reported in the native region. That circumstantial evidence along with direct evidence showing A. variglandis prevalence to be six times greater in non-native vs. native populations seems to suggest a significant influence on disease dynamics in west coast populations, which requires further investigation.
I have also explored the population genetics of H. sanguineus in its native and non-native region, collaborating with colleagues from VA SeaGrant (Susan Park) and Japan (Osamu Miura), as well as a local high school student (Jaclyn Onufrey). Hemigrapsus sanguineus is now the most common shorecrab in many areas of the eastern US; even so, nothing is yet known about genetic connections and possible source locations for its N. American introduction. Using a historical data set collected by S. Park in 1999-2001 of native (China, Japan, Korea) and non-native populations (Maine to Delaware), along with many of the same populations in recent years (2013-2014), we explored the effect of time on the crab’s population genetics in both regions, while also resolving source regions for its US introduction. Our work finds evidence for multiple introductions over time; moreover, my student Jaclyn submitted a paper based on this work (and other evidence) to the National Intel Competition, and she was named a 2014 semi-finalist—a tremendous honor for us both, and the first time anyone in her school had ever reached that level in a national competition.
In 2014, I spent a month in Scotland with a colleague from the Univ of St. Andrews (Anna Kintner) as part of a funded project on a cosmopolitan hydroid species, Obelia geniculata. We were interested in the gene flow and migration of this species, which has become a nuisance to Scottish salmon farmers in its medusa stage because it can access mariculture pens and harm fish. I am co-PI on this project which was funded by the Marine Alliance for Science and Technology Scotland (MASTS) as part of a research exchange. Anna and I sampled from populations throughout northern Scotland, and then we took our samples to the US, where she worked in my lab to prepare them for sequencing. We are currently analyzing our resulting genetic data, exploring the species’ population structure and gene flow along Scottish coasts.
I am also finalizing analyses on a host-parasite population genetics study in the eastern mudsnail, Ilyanassa obsoleta, introduced to the N. American west coast in the early 1900s, where it is infected by a subset of its native parasite diversity (Blakeslee et al., 2012, J. Biogeog.). My results demonstrate a differential effect of introduction on genetic diversity in the host snail compared to its parasites (Blakeslee et al., in prep), likely due to inherent differences in host-parasite life histories, vector propagule pressure, and survivorship, leading to greater genetic bottlenecks in the parasites. In the future, I would like to investigate other hosts, particularly west coast natives, because the addition of new parasites to the region is likely influencing community interactions. For example, the trematode Austrobilharzia variglandis has been implicated in outbreaks of swimmer’s itch in some west coast communities where I. obsoleta is invasive but is rarely reported in the native region. That circumstantial evidence along with direct evidence showing A. variglandis prevalence to be six times greater in non-native vs. native populations seems to suggest a significant influence on disease dynamics in west coast populations, which requires further investigation.
I have also explored the population genetics of H. sanguineus in its native and non-native region, collaborating with colleagues from VA SeaGrant (Susan Park) and Japan (Osamu Miura), as well as a local high school student (Jaclyn Onufrey). Hemigrapsus sanguineus is now the most common shorecrab in many areas of the eastern US; even so, nothing is yet known about genetic connections and possible source locations for its N. American introduction. Using a historical data set collected by S. Park in 1999-2001 of native (China, Japan, Korea) and non-native populations (Maine to Delaware), along with many of the same populations in recent years (2013-2014), we explored the effect of time on the crab’s population genetics in both regions, while also resolving source regions for its US introduction. Our work finds evidence for multiple introductions over time; moreover, my student Jaclyn submitted a paper based on this work (and other evidence) to the National Intel Competition, and she was named a 2014 semi-finalist—a tremendous honor for us both, and the first time anyone in her school had ever reached that level in a national competition.
In 2014, I spent a month in Scotland with a colleague from the Univ of St. Andrews (Anna Kintner) as part of a funded project on a cosmopolitan hydroid species, Obelia geniculata. We were interested in the gene flow and migration of this species, which has become a nuisance to Scottish salmon farmers in its medusa stage because it can access mariculture pens and harm fish. I am co-PI on this project which was funded by the Marine Alliance for Science and Technology Scotland (MASTS) as part of a research exchange. Anna and I sampled from populations throughout northern Scotland, and then we took our samples to the US, where she worked in my lab to prepare them for sequencing. We are currently analyzing our resulting genetic data, exploring the species’ population structure and gene flow along Scottish coasts.
(4) Community Ecology and Host-Parasite Interactions: Although parasites make up a large proportion of species abundance in many systems, they are often overlooked as a major contributor to population and community level dynamics. I am interested in better understanding the ecological, evolutionary, and environmental influences of parasites in native and introduced communities, as well as their distributions and interactions with hosts. In prior work with colleagues, I contributed to research on the behavioral effects of parasites on community structure (Wood et al. 2007) and influential factors (biological / physical) determining parasitism in snail hosts (Byers et al. 2008). In fact, regarding this latter effort, in 2013 we revisited this 11-year old study (Byers et al., 2008) with an undergraduate summer intern to explore temporal effects of trematode prevalence at a biogeographic scale and their correlations with definitive host abundance. The resulting manuscript was recently published in Ecology (Byers et al. 2016).
I have also investigated the influence of parasitism on the physiology and behavior of the green crab (C. maenas), which serves as a second-intermediate host to a common trematode species. We found some evidence for physiological and behavioral impacts on the crab, and our baseline effort was the first attempt to understand multiple effects of trematode parasitism on C. maenas. Our work represents an essential step in determining whether parasitism could be a likely influence on the crab’s interactions with numerous N. American coastal species (Blakeslee et al. 2015, PLOS One). We hope to expand this effort and explore community interactions involving other hosts and competitors.
I have also investigated the influence of parasitism on the physiology and behavior of the green crab (C. maenas), which serves as a second-intermediate host to a common trematode species. We found some evidence for physiological and behavioral impacts on the crab, and our baseline effort was the first attempt to understand multiple effects of trematode parasitism on C. maenas. Our work represents an essential step in determining whether parasitism could be a likely influence on the crab’s interactions with numerous N. American coastal species (Blakeslee et al. 2015, PLOS One). We hope to expand this effort and explore community interactions involving other hosts and competitors.
