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

Ecology and evolution of invasive plants: what to study next?

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

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

Molecular Detection of Invasive Species in Heterogeneous Mixtures Using a Microfluidic Carbon Nanotube Platform

Screening methods to prevent introductions of invasive species are critical for the protection of environmental and economic benefits provided by native species and uninvaded ecosystems. Coastal ecosystems worldwide remain vulnerable to damage from aquatic species introductions, particularly via ballast water discharge from ships. Because current ballast management practices are not completely effective, rapid and sensitive screening methods are needed for on-site testing of ships in transit. Here, we describe a detection technology based on a microfluidic chip containing DNA oligonucleotide functionalized carbon nanotubes. We demonstrate the efficacy of the chip using three ballast-transported species either established (Dreissena bugensis) or of potential threat (Eriocheir sinensis and Limnoperna fortuneii) to the Laurentian Great Lakes. With further refinement for on-board application, the technology could lead to real-time ballast water screening to improve ship-specific management and control decisions

Standing genetic diversity and selection at functional gene loci are associated with differential invasion success in two non‐native fish species

Invasive species are expected to experience a unique combination of high genetic drift due to demographic factors while also experiencing strong selective pressures. The paradigm that reduced genetic diversity should limit the evolutionary potential of invasive species and thus their potential for range expansion has received little empirical support, possibly due to the choice of genetic markers. Our goal was to test for effects of genetic drift and selection at functional genetic markers as they relate to the invasion success of two paired invasive goby species, one widespread (successful) and one with limited range expansion (less successful). We genotyped fish using two marker types: single nucleotide polymorphisms (SNPs) in known-function, protein-coding genes and microsatellites to contrast the effects of neutral genetic processes. We identified reduced allelic variation in the invaded range for the less-successful tubenose goby. SNPs putatively under selection were responsible for the observed differences in population structure between marker types for round goby (successful) but not tubenose goby (less successful). A higher proportion of functional loci experienced divergent selection for round goby, suggesting increased evolutionary potential in invaded ranges may be associated with round goby’s greater invasion success. Genes involved in thermal tolerance were divergent for round goby populations but not tubenose goby, consistent with the hypothesis that invasion success for fish in temperate regions is influenced by capacity for thermal tolerance. Our results highlight the need to incorporate functional genetic markers in studies to better assess evolutionary potential for the improved conservation and management of species

Development and Application of Microsatellites in Carcinus maenas: Genetic Differentiation between Northern and Central Portuguese Populations

Carcinus maenas, the common shore crab of European coastal waters, has recently gained notoriety due to its globally invasive nature associated with drastic ecological and economic effects. The native ubiquity and worldwide importance of C. maenas has resulted in it becoming one of the best-studied estuarine crustacean species globally. Accordingly, there is significant interest in investigating the population genetic structure of this broadly distributed crab along European and invaded coastlines. Here, we developed polymerase chain reaction (PCR) primers for one dinucleotide and two trinucleotide microsatellite loci, resulting from an enrichment process based on Portuguese populations. Combining these three new markers with six existing markers, we examined levels of genetic diversity and population structure of C. maenas in two coastal regions from Northern and Central Portugal. Genotypes showed that locus polymorphism ranged from 10 to 42 alleles (N = 135) and observed heterozygosity per locus ranged from 0.745 to 0.987 with expected heterozygosity ranging from 0.711 to 0.960; values typical of marine decapods. The markers revealed weak, but significant structuring among populations (global FST = 0.004) across a 450 km (over-water distance) spatial scale. Combinations of these and existing markers will be useful for studying population genetic parameters at a range of spatial scales of C. maenas throughout its expanding species range