Tepolt
Carolyn K.
Tepolt
Carolyn K.
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ArticleCurrent research, pressing issues, and lingering questions in marine invasion science: lessons from the Tenth International Conference on Marine Bioinvasions (ICMB-X)(Regional Euro-Asian Biological Invasions Centre, 2020-03-21) Fowler, Amy E. ; Blakeslee, April M. H. ; Bortolus, Alejandro ; Dias, P. Joana ; Tepolt, Carolyn K. ; Schwindt, EvangelinaResearch on marine bioinvasions is an inherently international collaboration. Species range boundaries have become more fluid in recent decades as a result of enhanced human globalization, leading to species translocations across international boundaries through high profile vectors (e.g., shipping, hull fouling, aquaculture, etc.) (Ruiz et al. 2000; Seebens et al. 2013). Global trade and anthropogenic activities that promote invasive species spread continue to increase, rising by an average of 70% since 1970, with no sign of saturation (Pagad et al. 2015; Seebens et al. 2017). Even though these numbers are primarily based on terrestrial systems, recent work has demonstrated that marine ecosystems are as severely impacted by invasive species as by other human activities including overfishing, pollution (including plastics), climate change, and ocean acidification (Diaz et al. 2019). Species introductions to seas, coasts, and estuaries are therefore a global threat to human and non-human populations alike. As such, scientists and managers are increasingly focused on prevention and management, risk analysis and prioritization, and innovative technologies to detect novel species.
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ArticleRecent introductions reveal differential susceptibility to parasitism across an evolutionary mosaic(Wiley Open Access, 2019-09-04) Tepolt, Carolyn K. ; Darling, John A. ; Blakeslee, April M. H. ; Fowler, Amy E. ; Torchin, Mark ; Miller, A. Whitman ; Ruiz, GregoryParasitism can represent a potent agent of selection, and introduced parasites have the potential to substantially alter their new hosts' ecology and evolution. While significant impacts have been reported for parasites that switch to new host species, the effects of macroparasite introduction into naïve populations of host species with which they have evolved remain poorly understood. Here, we investigate how the estuarine white‐fingered mud crab (Rhithropanopeus harrisii ) has adapted to parasitism by an introduced rhizocephalan parasite (Loxothylacus panopaei ) that castrates its host. While the host crab is native to much of the East and Gulf Coasts of North America, its parasite is native only to the southern end of this range. Fifty years ago, the parasite invaded the mid‐Atlantic, gradually expanding through previously naïve host populations. Thus, different populations of the same host species have experienced different degrees of historical interaction (and thus potential evolutionary response time) with the parasite: long term, short term, and naïve. In nine estuaries across this range, we examined whether and how parasite prevalence and host susceptibility to parasitism differs depending on the length of the host's history with the parasite. In field surveys, we found that the parasite was significantly more prevalent in its introduced range (i.e., short‐term interaction) than in its native range (long‐term interaction), a result that was also supported by a meta‐analysis of prevalence data covering the 50 years since its introduction. In controlled laboratory experiments, host susceptibility to parasitism was significantly higher in naïve hosts than in hosts from the parasite's native range, suggesting that host resistance to parasitism is under selection. These results suggest that differences in host–parasite historical interaction can alter the consequences of parasite introductions in host populations. As anthropogenically driven range shifts continue, disruptions of host–parasite evolutionary relationships may become an increasingly important driver of ecological and evolutionary change.
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ArticleLatitudinal and temporal variation in injury and its impacts in the invasive Asian shore crab Hemigrapsus sanguineus(Nature Research, 2022-10-03) Griffen, Blaine D ; Alder, Jill ; Anderson, Lars ; Asay, Emily Gail ; Blakeslee, April ; Bolander, Mikayla ; Cabrera, Doreen ; Carver, Jade ; Crane, Laura C ; DiNuzzo, Eleanor R ; Fletcher, Laura S ; Luckett, Johanna ; Meidell, Morgan ; Pinkston, Emily ; Reese, Tanner C ; Repetto, Michele F ; Smith, Nanette ; Stancil, Carter ; Tepolt, Carolyn K ; Toscano, Benjamin J ; Vernier, AshleyNonlethal injury is a pervasive stress on individual animals that can affect large portions of a population at any given time. Yet most studies examine snapshots of injury at a single place and time, making the implicit assumption that the impacts of nonlethal injury are constant. We sampled Asian shore crabsHemigrapsus sanguineusthroughout their invasive North American range and from the spring through fall of 2020. We then documented the prevalence of limb loss over this space and time. We further examined the impacts of limb loss and limb regeneration on food consumption, growth, reproduction, and energy storage. We show that injury differed substantially across sites and was most common towards the southern part of their invaded range on the East Coast of North America. Injury also varied idiosyncratically across sites and through time. It also had strong impacts on individuals via reduced growth and reproduction, despite increased food consumption in injured crabs. Given the high prevalence of nonlethal injury in this species, these negative impacts of injury on individual animals likely scale up to influence population level processes (e.g., population growth), and may be one factor acting against the widespread success of this invader.
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ArticleRapid adaptation to temperature via a potential genomic island of divergence in the invasive green crab, Carcinus maenas(Frontiers Media, 2020-11-26) Tepolt, Carolyn K. ; Palumbi, Stephen R.Widespread species often adapt easily to novel conditions – both those found in new habitats and those generated by climate change. However, rapid adaptation may be hindered in the marine realm, where long-distance dispersal and consequently high gene flow are predicted to limit potential for local adaptation. Here, we use a highly dispersive invasive marine crab to test the nature and speed of adaptation to temperature in the sea. Using single nucleotide polymorphisms (SNPs) generated from cardiac transcriptome sequencing, we characterized six populations of the European green crab (Carcinus maenas) located across parallel thermal gradients in their native and invasive ranges. We compared SNP frequencies with local temperatures and previously generated data on cardiac heat and cold tolerance to identify candidate markers associated with population-level differences in thermal physiology. Of 10,790 SNPs, 104 were identified as frequency outliers, a signal that was strongly driven by association with temperature and/or cold tolerance. Seventy-two of these outlier markers, representing 28 different genes, were in a cluster of SNPs identified as a potential inversion polymorphism using linkage disequilibrium network analysis. This SNP cluster was unique in the data set, which was otherwise characterized by low levels of linkage disequilibrium, and markers in this cluster showed a significant enrichment of coding substitutions relative to the full SNP set. These 72 outlier SNPs appear to be transmitted as a unit, and represent a putative genomic island of divergence which varied in frequency with organismal cold tolerance. This relationship was strikingly similar across both native and invasive populations, all of which showed a very strong correlation with cold tolerance (R2 = 0.96 over all six populations). Notably, three of these populations have diverged recently (<100 years) and show little to no neutral divergence, suggesting that this genomic region may be responding to temperature on a relatively short time scale. This relationship indicates adaptation to temperature based on the action of a putative genomic island of divergence, perhaps partially explaining the extraordinary invasive ability of this species.
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ArticleAn evolutionary perspective on marine invasions(Wiley, 2019-12-16) Blakeslee, April M. H. ; Manousaki, Tereza ; Vasileiadou, Katerina ; Tepolt, Carolyn K.Species distributions are rapidly changing as human globalization increasingly moves organisms to novel environments. In marine systems, species introductions are the result of a number of anthropogenic mechanisms, notably shipping, aquaculture/mariculture, the pet and bait trades, and the creation of canals. Marine invasions are a global threat to human and non‐human populations alike and are often listed as one of the top conservation concerns worldwide, having ecological, evolutionary, and social ramifications. Evolutionary investigations of marine invasions can provide crucial insight into an introduced species’ potential impacts in its new range, including: physiological adaptation and behavioral changes to exploit new environments; changes in resident populations, community interactions, and ecosystems; and severe reductions in genetic diversity that may limit evolutionary potential in the introduced range. This special issue focuses on current research advances in the evolutionary biology of marine invasions and can be broadly classified into a few major avenues of research: the evolutionary history of invasive populations, post‐invasion reproductive changes, and the role of evolution in parasite introductions. Together, they demonstrate the value of investigating marine invasions from an evolutionary perspective, with benefits to both fundamental and applied evolutionary biology at local and broad scales.
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ArticleMitochondrial genotype influences the response to cold stress in the European green crab Carcinus maenas(Company of Biologists, 2019-07-08) Coyle, Aidan F. ; Voss, Erin R. ; Tepolt, Carolyn K. ; Carlon, David B.Hybrid zones provide natural experiments in recombination within and between genomes that may have strong effects on organismal fitness. On the East Coast of North America, two distinct lineages of the European green crab (Carcinus maenas) have been introduced in the last two centuries. These two lineages with putatively different adaptive properties have hybridized along the coast of the eastern Gulf of Maine, producing new nuclear and mitochondrial combinations that show clinal variation correlated with water temperature. To test the hypothesis that mitochondrial or nuclear genes have effects on thermal tolerance, we first measured the response to cold stress in crabs collected throughout the hybrid zone, then sequenced the mitochondrial CO1 gene and two nuclear single nucleotide polymorphisms (SNPs) representative of nuclear genetic lineage. Mitochondrial haplotype had a strong association with the ability of crabs to right themselves at 4.5°C that was sex specific: haplotypes originally from northern Europe gave male crabs an advantage while there was no haplotype effect on righting in female crabs. By contrast, the two nuclear SNPs that were significant outliers in a comparison between northern and southern C. maenas populations had no effect on righting response at low temperature. These results add C. maenas to the shortlist of ectotherms in which mitochondrial variation has been shown to affect thermal tolerance, and suggest that natural selection is shaping the structure of the hybrid zone across the Gulf of Maine. Our limited genomic sampling does not eliminate the strong possibility that mito-nuclear co-adaptation may play a role in the differences in thermal phenotypes documented here. Linkage between mitochondrial genotype and thermal tolerance suggests a role for local adaptation in promoting the spread of invasive populations of C. maenas around the world.
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ArticleEffects of season and latitude on the diet quality of the invasive Asian shore crab Hemigrapsus sanguineus(Inter Research, 2023-01-26) Reese, Tanner C. ; Alder, Jill ; Asay, Emily Gail ; Blakeslee, April M. H. ; Cabrera, Doreen ; Crane, Laura C. ; Fletcher, Laura S. ; Pinkston, Emily ; Repetto, Michele F. ; Smith, Nanette ; Stancil, Carter ; Tepolt, Carolyn K. ; Toscano, Benjamin J. ; Griffen, Blaine D.Invasive species alter invaded ecosystems via direct impacts such as consumption. In turn, an invasive species’ ability to thrive in new habitats depends on its ability to exploit available resources, which may change over time and space. Diet quality and quantity are indicators of a consumer’s consumptive effects and can be strongly influenced by season and latitude. We examined the effects of season and latitude on the diet quality and quantity of the invasive Asian shore crab Hemigrapsus sanguineus throughout a non-winter sampling year at 5 different sites spanning 8° of latitude across its invaded United States range. We found that diet quality, averaged through time, largely follows an expected latitudinal cline, being higher in the center of its range and lower toward the southern and northern edges. We also found that while some sites show similar patterns of diet quality variation with season, no pattern is consistent across all latitudes. Finally, we found that crabs at sites with low diet quality during summer reproductive months did not compensate by increasing total consumption. Because the Asian shore crab is an important consumer in its invaded ecosystems, understanding how its diet quality and quantity vary with season and latitude can help us better understand how this species influences trophic interactions and community structure, how it has been able to establish across a wide ecological and environmental range, and where future range expansion is most likely to occur.
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ArticleParasite diversity at isolated, disturbed hydrothermal vents(The Royal Society, 2023-06-14) Dykman Lauren ; Tepolt, Carolyn K. ; Kuris, Armand M. ; Solow, Andrew R. ; Mullineaux, Lauren S.Habitat isolation and disturbance are important regulators of biodiversity, yet it remains unclear how these environmental features drive differences in parasite diversity between ecosystems. We test whether the biological communities in an isolated, frequently disturbed marine ecosystem (deep-sea hydrothermal vents) have reduced parasite richness and relatively fewer parasite species with indirect life cycles (ILCs) compared to ecosystems that are less isolated and less disturbed. We surveyed the parasite fauna of the biological community at the 9°50′N hydrothermal vent field on the East Pacific Rise and compared it to similar datasets from a well-connected and moderately disturbed ecosystem (kelp forest) and an isolated and undisturbed ecosystem (atoll sandflat). Parasite richness within host species did not differ significantly between ecosystems, yet total parasite richness in the vent community was much lower due to the low number of predatory fish species. Contrary to expectation, the proportion of ILC parasite species was not lower at vents due to a high richness of trematodes, while other ILC parasite taxa were scarce (nematodes) or absent (cestodes). These results demonstrate the success of diverse parasite taxa in an extreme environment and reinforce the importance of host diversity and food web complexity in governing parasite diversity.
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ArticlePast energy allocation overwhelms current energy stresses in determining energy allocation trade-offs(Wiley Open Access, 2023-08-08) Griffen, Blaine D. ; Bolander, Mikayla ; Blakeslee, April ; Crane, Laura C. ; Repetto, Michele F. ; Tepolt, Carolyn K. ; Toscano, Benjamin J.Regeneration of lost appendages is a gradual process in many species, spreading energetic costs of regeneration through time. Energy allocated to the regeneration of lost appendages cannot be used for other purposes and, therefore, commonly elicits energetic trade-offs in biological processes. We used limb loss in the Asian shore crab Hemigrapsus sanguineus to compare the strength of energetic trade-offs resulting from historic limb losses that have been partially regenerated versus current injuries that have not yet been repaired. Consistent with previous studies, we show that limb loss and regeneration results in trade-offs that reduce reproduction, energy storage, and growth. As may be expected, we show that trade-offs in these metrics from historic limb losses far outweigh trade-offs from current limb losses, and correlate directly with the degree of historic limb loss that has been regenerated. As regenerating limbs get closer to their normal size, these historical injuries get harder to detect, despite the continued allocation of additional resources to limb development. Our results demonstrate the importance of and a method for identifying historic appendage losses and of quantifying the amount of regeneration that has already occurred, as opposed to assessing only current injury, to accurately assess the strength of energetic trade-offs in animals recovering from nonlethal injury.
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ArticleConcentration and condition of American lobster postlarvae in small-scale convergences(Wiley, 2023-10-11) Pineda, Jesus ; Tepolt, Carolyn K. ; Starczak, Vicke ; Alatalo, Phil ; Shapiro, SaraInvertebrate larvae are often abundant in the surface ocean, which plays a key role in their dispersal and connectivity. Pelagic microhabitats characterized by small-scale hydrographic variability are complex and ubiquitous in the coastal ocean, but their study is challenging, and they have been largely neglected in meroplankton ecology. Surface convergences, i.e., surface microhabitats featuring convergent horizontal currents, may aggregate the last larval stage of the American lobster and could provide shelter and food for Stage IV postlarvae and thus enhance their condition. We tested these hypotheses by conducting a series of cruises in the southwestern Gulf of Maine in summer 2021, sampling 15 paired sets of potential convergences and off-convergence unstructured habitat. We measured postlarval abundance, surface hydrography, acoustic backscatter, and circulation. Experiments and image analysis compared condition, color, and morphology of postlarvae sampled inside and outside potential convergences. Potential convergences varied in near-surface hydrographic patterns, with most displaying consistency among two transects and diverse patterns in salinity and temperature (e.g., across-convergence gradients with equal or different signs). While the highest postlarval abundances were found in convergences, abundance patterns on and off convergences were not consistent, and another analysis indicated higher abundance in convergences than in a 7-year untargeted surface ocean data set. Experiments indicated no survivorship differences among convergence and non-convergence individuals at two temperatures, while image analyses revealed differences in color and size. Physical measurements and qualitative neuston community analyses indicated substantial heterogeneity among potential convergences. Our results reinforce that small-scale heterogeneities are highly variable but important to the ecology of meroplankton, including the pelagic and neustonic habitats where lobster postlarvae are abundant.