Rapid adaptation to temperature via a potential genomic island of divergence in the invasive green crab, Carcinus maenas

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Tepolt, C. K., & Palumbi, S. R. Rapid adaptation to temperature via a potential genomic island of divergence in the invasive green crab, Carcinus maenas. Frontiers in Ecology and Evolution, 8, (2020): 580701, doi:10.3389/fevo.2020.580701.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.CT was supported on this project by a National Defense Science and Engineering Grant, a Stanford Graduate Fellowship, a Stanford Center for Computational, Evolutionary, and Human Genomics Fellowship, and the Penzance Endowed Fund in Support of Assistant Scientists at WHOI. The sampling and sequencing of the data used in this analysis was funded by the Partnership for the Interdisciplinary Study of Coastal Oceans, the Myers Trust, the Explorer’s Club Exploration Fund, the Lerner Gray Memorial Fund of the American Museum of Natural History, the Vice Provost for Graduate Education at Stanford, the Eugene C. and Aileen E. Haderlie Memorial Fund, and a National Science Foundation Doctoral Dissertation Improvement Grant (1210057)

An evolutionary perspective on marine invasions

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

Mitochondrial genotype influences the response to cold stress in the European green crab Carcinus maenas

Author Posting. © Company of Biologists, 2019. This article is posted here by permission of Company of Biologists for personal use, not for redistribution. The definitive version was published in Journal of Experimental Biology 222(17), (2019):jeb.20352, doi: 10.1242/jeb.203521.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.We would like to thank T. Suskiewicz and L. Johnson for help collecting crabs from Halifax, NS, and Robin Seeley for collections from the Isle of Shoals. We thank Timothy Fuller for designing and testing the SMC primers. We thank Mark Murray for facilitating a productive stay on Kent Island, and Nick Keeney for assistance with animal care at the Schiller Coastal Studies Center. This is publication no. 5 from the Bowdoin Marine Laboratory.2020-07-0

Current research, pressing issues, and lingering questions in marine invasion science: lessons from the Tenth International Conference on Marine Bioinvasions (ICMB-X)

© The Author(s), 2020. This article is distributed under the terms of the Creative Commons Attribution License. The definitive version was published in Fowler, A. E., Blakeslee, A. M. H., Bortolus, A., Dias, J., Tepolt, C. K., & Schwindt, E. Current research, pressing issues, and lingering questions in marine invasion science: lessons from the Tenth International Conference on Marine Bioinvasions (ICMB-X). Aquatic Invasions, 15(1), (2020): 1-10, doi:10.3391/ai.2020.15.1.01.Research 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.The ICMB-X was supported by CONICET, MINCyT, SCTeIP Chubut, Consejo Federal de Inversiones, Biodiversity Heritage Library, Administración Portuaria de Puerto Madryn (APPM), Office of Naval Research Global, Aluar Aluminio Argentino, Madryn Bureau, Ente Mixto Puerto Madryn, Municipalidad de Puerto Madryn, and FAO-GEF-SAyDS

Linking concepts in the ecology and evolution of invasive plants: network analysis shows what has been most studied and identifies knowledge gaps

In recent decades, a growing number of studies have addressed connections between ecological and evolutionary concepts in biologic invasions. These connections may be crucial for understanding the processes underlying invaders’ success. However, the extent to which scientists have worked on the integration of the ecology and evolution of invasive plants is poorly documented, as few attempts have been made to evaluate these efforts in invasion biology research. Such analysis can facilitate recognize well-documented relationships and identify gaps in our knowledge. In this study, we used a network-based method for visualizing the connections between major aspects of ecology and evolution in the primary research literature. Using the family Poaceae as an example, we show that ecological concepts were more studied and better interconnected than were evolutionary concepts. Several possible connections were not documented at all, representing knowledge gaps between ecology and evolution of invaders. Among knowledge gaps, the concepts of plasticity, gene flow, epigenetics and human influence were particularly under-connected. We discuss five possible research avenues to better understand the relationships between ecology and evolution in the success of Poaceae, and of alien plants in general

Genomic Tools in Biological Invasions: Current State and Future Frontiers

Human activities are accelerating rates of biological invasions and climate-driven range expansions globally, yet we understand little of how genomic processes facilitate the invasion process. Although most of the literature has focused on underlying phenotypic correlates of invasiveness, advances in genomic technologies are showing a strong link between genomic variation and invasion success. Here, we consider the ability of genomic tools and technologies to (i) inform mechanistic understanding of biological invasions and (ii) solve real-world issues in predicting and managing biological invasions. For both, we examine the current state of the field and discuss how genomics can be leveraged in the future. In addition, we make recommendations pertinent to broader research issues, such as data sovereignty, metadata standards, collaboration, and science communication best practices that will require concerted efforts from the global invasion genomics community

Potentially non-neutral SNPs for Carcinus maenas

List of SNPs determined to be potentially non-neutral in Carcinus maenas. Codes as given in associated assembly and genotype data

Data from: Transcriptome sequencing reveals both neutral and adaptive genome dynamics in a marine invader

Species invasions cause significant ecological and economic damage, and genetic information is important to understanding and managing invasive species. In the ocean, many invasive species have high dispersal and gene flow, lowering the discriminatory power of traditional genetic approaches. High-throughput sequencing holds tremendous promise for increasing resolution and illuminating the relative contributions of selection and drift in marine invasion, but has not yet been used to compare the diversity and dynamics of a high-dispersal invader in its native and invaded ranges. We test a transcriptome-based approach in the European green crab (Carcinus maenas), a widespread invasive species with high gene flow and a well-known invasion history, in two native and five invasive populations. A panel of 10 809 transcriptome-derived nuclear SNPs identified significant population structure among highly bottlenecked invasive populations that were previously undifferentiated with traditional markers. Comparing the full data set and a subset of 9246 putatively neutral SNPs strongly suggested that non-neutral processes are the primary driver of population structure within the species’ native range, while neutral processes appear to dominate in the invaded range. Non-neutral native range structure coincides with significant differences in intraspecific thermal tolerance, suggesting temperature as a potential selective agent. These results underline the importance of adaptation in shaping intraspecific differences even in high geneflow marine invasive species. They also demonstrate that high-throughput approaches have broad utility in determining neutral structure in recent invasions of such species. Together, neutral and non-neutral data derived from high-throughput approaches may increase the understanding of invasion dynamics in high-dispersal species

Nuclear SNP genotypes for Carcinus maenas

Individual genotypes for 84 Carcinus maenas individuals from seven sites in the native and invasive ranges. Genotypes given for 10,809 high-quality nuclear SNPs. Further detail in associated publications

Putatively neutral SNPs for Carcinus maenas

List of SNPs determined to be putatively neutral in Carcinus maenas. Codes as given in associated assembly and genotype data