John A. Darling

From molecules to management: Adopting DNA-based methods for monitoring biological invasions in aquatic environments ☆

Recent technological advances have driven rapid development of DNA-based methods designed to facilitate detection and monitoring of invasive species in aquatic environments. These tools promise to improve on traditional monitoring approaches by enhancing detection sensitivity, reducing analytical turnaround times and monitoring costs, and increasing specificity of target identifications. However, despite the promise of DNA-based monitoring methods, the adoption of these tools in decision-making frameworks remains challenging. Here, rather than explore technical aspects of method development, we examine impediments to effective translation of those methods into management contexts. In addition to surveying current use of DNA-based tools for aquatic invasive species monitoring, we explore potential sources of uncertainty associated with molecular technologies and possibilities for limiting that uncertainty and effectively communicating its implications for decision-making. We pay particular attention to the recent adoption of DNA-based methods for detection of invasive Asian carp species in the United States Great Lakes region, as this example illustrates many of the challenges associated with applying molecular tools to achieve desired management outcomes. Our goal is to provide a useful assessment of the obstacles associated with integrating DNA-based methods into aquatic invasive species management, and to offer recommendations for future efforts aimed at overcoming those obstacles.

Genetic patterns across multiple introductions of the globally invasive crab genus Carcinus

The European green crab Carcinus maenas is one of the worlds most successful aquatic invaders, having established populations on every continent with temperate shores. Here we describe patterns of genetic diversity across both the native and introduced ranges of C. maenas and its sister species, C. aestuarii, including all known non‐native populations. The global data set includes sequences from the mitochondrial cytochrome c oxidase subunit I gene, as well as multilocus genotype data from nine polymorphic nuclear microsatellite loci. Combined phylogeographic and population genetic analyses clarify the global colonization history of C. maenas, providing evidence of multiple invasions to Atlantic North America and South Africa, secondary invasions to the northeastern Pacific, Tasmania, and Argentina, and a strong likelihood of C. maenas × C. aestuarii hybrids in South Africa and Japan. Successful C. maenas invasions vary broadly in the degree to which they retain genetic diversity, although populations with the least variation typically derive from secondary invasions or from introductions that occurred more than 100 years ago.

How important is intraspecific genetic admixture to the success of colonising populations

Genetic admixture of divergent intraspecific lineages is increasingly suspected to have an important role in the success of colonising populations. However, admixture is not a universally beneficial genetic phenomenon. Selection is typically expected to favour locally adapted genotypes and can act against admixed individuals, suggesting that there are some conditions under which admixture will have negative impacts on population fitness. Therefore, it remains unclear how often admixture acts as a true driver of colonisation success. Here, we review the population consequences of admixture and discuss its costs and benefits across a broad spectrum of ecological contexts. We critically evaluate the evidence for a causal role of admixture in successful colonisation, and consider that role more generally in driving population range expansion.

DNA-based methods for monitoring invasive species: a review and prospectus

The recent explosion of interest in DNA-based tools for species identification has prompted widespread speculation on the future availability of inexpensive, rapid, and accurate means of identifying specimens and assessing biodiversity. One applied field that may benefit dramatically from the development of such technologies is the detection, identification, and monitoring of invasive species. Recent studies have demonstrated the feasibility of DNA-based tools for such important tasks as confirmation of specimen identity and targeted screening for known or anticipated invaders. However, significant technological hurdles must be overcome before more ambitious applications, including estimation of propagule pressure and comprehensive surveys of complex environmental samples, are to be realized. Here we review existing methods, examine the technical difficulties associated with development of more sophisticated tools, and consider the potential utility of these DNA-based technologies for various applications relevant to invasive species monitoring.

Genetic analysis reveals multiple cryptic invasive species of the hydrozoan genus Cordylophora.

Understanding the patterns and dynamics of biological invasions is a crucial prerequisite to predicting and mitigating their potential ecological and economic impacts. Unfortunately, in many cases such understanding is limited not only by ignorance of invasion history, but also by uncertainty surrounding the ecology, physiology, and even systematics of the invasive taxa themselves. The invasive, colonial euryhaline hydroid Cordylophora has invaded multiple regions outside of its native Ponto-Caspian range. However, extensive morphological and ecological plasticity has prevented consensus on both species-level classification within the genus and the environmental conditions conducive to establishment. The goal of this research was to explore the invasive history and species composition of the genus Cordylophora through molecular analyses. We addressed both issues using DNA sequence data from two mitochondrial loci [the small subunit 16S rRNA and cytochrome c oxidase subunit I (COI)] and one nuclear locus (28S large nuclear rRNA), generated from 27 invasive Cordylophora populations collected throughout the global range of the taxon. Phylogenetic analysis and comparisons of genetic distances between populations suggest the presence of multiple cryptic species within the genus. This conclusion is further supported by the observation of significantly different habitat preferences between invasive lineages. Geographic distribution of lineages is consistent with the introduction of multiple lineages to some non-native regions, indicating that repeated introductions may contribute to the current global distribution of Cordylophora. Applying molecular and morphological analyses to additional populations of Cordylophora is likely to assist in clarifying the taxonomy of this genus and in providing a better understanding of the invasive history of this hydroid.

The Quagga Mussel Invades the Lake Superior Basin

ABSTRACT Prior studies recognized the presence of a single dreissenid species in Lake Superior—the zebra mussel Dreissena polymorpha. However, taxonomic keys based on traditional shell morphology are not always able to differentiate dreissenid species with confidence. We thus employed genetic and morphological analyses to identify dreissenids in a major river-embayment of Lake Superior—the lower St. Louis River/Duluth-Superior Harbor—during 2005–2006. Our results revealed the presence of a second dreissenid species—the quagga mussel D. bugensis (alternatively known as D. rostriformis bugensis). Both species occurred in mixed clusters, in which zebra mussels outnumbered quagga mussels (20–160:1). The largest quagga mussel collected in 2005 was 26.5 mm long and estimated to be two years old, suggesting that the initial introduction occurred no later than 2003. Further monitoring is necessary to determine whether the quagga mussel will colonize Lake Superior. Our results indicate that the coupling of conventional morphological and molecular approaches is essential for monitoring dreissenid species.

Genetic analysis across different spatial scales reveals multiple dispersal mechanisms for the invasive hydrozoan Cordylophora in the Great Lakes.

Discerning patterns of post‐establishment spread by invasive species is critically important for the design of effective management strategies and the development of appropriate theoretical models predicting spatial expansion of introduced populations. The globally invasive colonial hydrozoan Cordylophora produces propagules both sexually and vegetatively and is associated with multiple potential dispersal mechanisms, making it a promising system to investigate complex patterns of population structure generated throughout the course of rapid range expansion. Here, we explore genetic patterns associated with the spread of this taxon within the North American Great Lakes basin. We collected intensively from eight harbours in the Chicago area in order to conduct detailed investigation of local population expansion. In addition, we collected from Lakes Michigan, Erie, and Ontario, as well as Lake Cayuga in the Finger Lakes of upstate New York in order to assess genetic structure on a regional scale. Based on data from eight highly polymorphic microsatellite loci we examined the spatial extent of clonal genotypes, assessed levels of neutral genetic diversity, and explored patterns of migration and dispersal at multiple spatial scales through assessment of population level genetic differentiation (pairwise FST and factorial correspondence analysis), Bayesian inference of population structure, and assignment tests on individual genotypes. Results of these analyses indicate that Cordylophora populations in this region spread predominantly through sexually produced propagules, and that while limited natural larval dispersal can drive expansion locally, regional expansion likely relies on anthropogenic dispersal vectors.

Complex genetic patterns in closely related colonizing invasive species

Anthropogenic activities frequently result in both rapidly changing environments and translocation of species from their native ranges (i.e., biological invasions). Empirical studies suggest that many factors associated with these changes can lead to complex genetic patterns, particularly among invasive populations. However, genetic complexities and factors responsible for them remain uncharacterized in many cases. Here, we explore these issues in the vase tunicate Ciona intestinalis (Ascidiacea: Enterogona: Cionidae), a model species complex, of which spA and spB are rapidly spreading worldwide. We intensively sampled 26 sites (N = 873) from both coasts of North America, and performed phylogenetic and population genetics analyses based on one mitochondrial fragment (cytochrome c oxidase subunit 3–NADH dehydrogenase subunit I, COX3-ND1) and eight nuclear microsatellites. Our analyses revealed extremely complex genetic patterns in both species on both coasts. We detected a contrasting pattern based on the mitochondrial marker: two major genetic groups in C. intestinalis spA on the west coast versus no significant geographic structure in C. intestinalis spB on the east coast. For both species, geo-graphically distant populations often showed high microsatellite-based genetic affinities whereas neighboring ones often did not. In addition, mitochondrial and nuclear markers provided largely inconsistent genetic patterns. Multiple factors, including random genetic drift associated with demographic changes, rapid selection due to strong local adaptation, and varying propensity for human-mediated propagule dispersal could be responsible for the observed genetic complexities.

Ecology of cryptic invasions: latitudinal segregation among Watersipora (Bryozoa) species

Watersipora is an invasive genus of bryozoans, easily dispersed by fouled vessels. We examined Cytochrome c oxidase subunit I haplotypes from introduced populations on the US Pacific coastline to investigate geographic segregation of species and/or haplotypes. In California, the W. subtorquata group fell into three major sub-groups: W. subtorquata clades A and B, and W. “new sp.”. W. subtorquata clades A and B were common in southern California south of Point Conception, a recognized biogeographic boundary, whereas further north, W. subtorquata clade A and W. n. sp. were frequent. The southern California region also had colonies of a morphologically distinct species, W. arcuata, also found in southern Australia and Hawaii; COI variation indicates a common ancestral source(s) in these introductions. The distribution of Watersipora-complex lineages on different coastlines is shown to be temperature correlated. Accordingly, pre-exisitng temperature-based adaptations may play a key role in determining invasion patterns.

Genetic studies of aquatic biological invasions: closing the gap between research and management.

Recent years have seen a dramatic rise in the application of genetic methods to understand aquatic biological invasions. In part these methods have been adopted to address fundamental questions in biogeography, evolutionary biology, population ecology, and other fields. But it is also commonly suggested that genetic information has the potential to directly inform the management of aquatic invasions. Here I explore the potential promise of genetic approaches for informing management of aquatic invasive species, the degree to which that promise has been realized in terms of utilization of genetic information by managers and other decision-makers, and the likely limitations to the value of genetic methods (both in principle and in practice) and ways in which these limitations might be overcome. I consider a range of possible applications of genetic tools for management, including molecular detection and identification of cryptic invaders, source tracking and reconstruction of invasion history, and inference of population demographics. Retrospective assessment of the utility of such applications is based on both literature review and solicitation of expert opinion, and suggests that a number of hurdles likely often prevent genetic information from effectively informing decision-making. These include (1) limitations or misunderstandings of the resolution and certainty afforded by genetic analysis; (2) failure to engage decision-makers in problem formulation, research design and research implementation; and (3) complex relationships between basic research and management actions. While some of the obstacles considered are rooted in theoretical and practical limitations of genetic analysis, others are clearly associated with poor communication and insufficient engagement of potential end-users of genetic information. I consider possible avenues for overcoming these obstacles and for improving the applicability of genetic information for supporting management decisions.