Gregory William Gelembiuk

Evolutionary origins of invasive populations

What factors shape the evolution of invasive populations? Recent theoretical and empirical studies suggest that an evolutionary history of disturbance might be an important factor. This perspective presents hypotheses regarding the impact of disturbance on the evolution of invasive populations, based on a synthesis of the existing literature. Disturbance might select for life‐history traits that are favorable for colonizing novel habitats, such as rapid population growth and persistence. Theoretical results suggest that disturbance in the form of fluctuating environments might select for organismal flexibility, or alternatively, the evolution of evolvability. Rapidly fluctuating environments might favor organismal flexibility, such as broad tolerance or plasticity. Alternatively, longer fluctuations or environmental stress might lead to the evolution of evolvability by acting on features of the mutation matrix. Once genetic variance is generated via mutations, temporally fluctuating selection across generations might promote the accumulation and maintenance of genetic variation. Deeper insights into how disturbance in native habitats affects evolutionary and physiological responses of populations would give us greater capacity to predict the populations that are most likely to tolerate or adapt to novel environments during habitat invasions. Moreover, we would gain fundamental insights into the evolutionary origins of invasive populations.

Evolution of Physiological Tolerance and Performance During Freshwater Invasions

Abstract Invasive species that penetrate habitat boundaries are likely to experience strong selection and rapid evolution. This study documents evolutionary shifts in tolerance and performance following the invasion of fresh water by the predominantly estuarine and salt marsh copepod Eurytemora affinis. Common-garden experiments were performed on freshwater-invading (Lake Michigan) and ancestral saline (St. Lawrence marsh) populations to measure shifts in adult survival (at 0, 5, and 25 PSU), and survival during development and development time (both using full-sib clutches split across 0, 5, 15, and 25 PSU). Results showed clear evidence of heritable shifts in tolerance and performance associated with freshwater invasions. The freshwater population exhibited a gain in low-salinity tolerance and a reduction in high-salinity tolerance relative to the saline population, suggesting tradeoffs. These tradeoffs were supported by negative genetic correlations between survival at fresh (0 PSU) versus higher salinities. Mortality in response to salinity occurred primarily before metamorphosis, suggesting that selection in response to salinity had acted primarily on the early life-history stages. The freshwater population exhibited curious patterns of life-history evolution across salinities, relative to the saline population, of retarded development to metamorphosis but accelerated development from metamorphosis to adulthood. This pattern might reflect tradeoffs between development rate and survival in fresh water at the early life-history stages, but some other selective force acting on later life-history stages. Significant effects of clutch (genotype) and clutch-by-salinity interaction (G × E) on survival and development time in both populations indicated ample genetic variation as substrate for natural selection. Variation for high-salinity tolerance was present in the freshwater population despite negative genetic correlations between high- and low-salinity tolerance. Results implicate the importance of natural selection and document the evolution of reaction norms during freshwater invasions.

PUMPING IONS: RAPID PARALLEL EVOLUTION OF IONIC REGULATION FOLLOWING HABITAT INVASIONS

Marine to freshwater colonizations constitute among the most dramatic evolutionary transitions in the history of life. This study examined evolution of ionic regulation following saline‐to‐freshwater transitions in an invasive species. In recent years, the copepod Eurytemora affinis has invaded freshwater habitats multiple times independently. We found parallel evolutionary shifts in ion‐motive enzyme activity (V‐type H+ ATPase, Na+/K+‐ATPase) across independent invasions and in replicate laboratory selection experiments. Freshwater populations exhibited increased V‐type H+ ATPase activity in fresh water (0 PSU) and declines at higher salinity (15 PSU) relative to saline populations. This shift represented marked evolutionary increases in plasticity. In contrast, freshwater populations displayed reduced Na+/K+‐ATPase activity across all salinities. Most notably, modifying salinity alone during laboratory selection experiments recapitulated the evolutionary shifts in V‐type H+ ATPase activity observed in nature. Maternal and embryonic acclimation could not account for the observed shifts in enzyme activity. V‐type H+ ATPase function has been hypothesized to be critical for freshwater and terrestrial adaptations, but evolution of this enzyme function had not been previously demonstrated in the context of habitat transitions. Moreover, the speed of these evolutionary shifts was remarkable, within a few generations in the laboratory and a few decades in the wild.

Molecular ecology of zebra mussel invasions

The invasion of the zebra mussel, Dreissena polymorpha, into North American waters has resulted in profound ecological disturbances and large monetary losses. This study examined the invasion history and patterns of genetic diversity among endemic and invading populations of zebra mussels using DNA sequences from the mitochondrial cytochrome oxidase I (COI) gene. Patterns of haplotype frequency indicate that all invasive populations of zebra mussels from North America and Europe originated from the Ponto‐Caspian Sea region. The distribution of haplotypes was consistent with invasive populations arising from the Black Sea drainage, but could not exclude the possibility of an origin from the Caspian Sea drainage. Similar haplotype frequencies among North American populations of D. polymorpha suggest colonization by a single founding population. There was no evidence of invasive populations arising from tectonic lakes in Turkey, while lakes in Greece and Macedonia contained only Dreissena stankovici. Populations in Turkey might be members of a sibling species complex of D. polymorpha. Ponto‐Caspian derived populations of D. polymorpha (θ = 0.0011) and Dreissena bugensis (one haplotype) exhibited low levels of genetic diversity at the COI gene, perhaps as a result of repeated population bottlenecks. In contrast, geographically isolated tectonic lake populations exhibited relatively high levels of genetic diversity (θ = 0.0032 to 0.0134). It is possible that the fluctuating environment of the Ponto‐Caspian basin facilitated the colonizing habit of invasive populations of D. polymorpha and D. bugensis. Our findings were concordant with the general trend of destructive freshwater invaders in the Great Lakes arising from the Ponto‐Caspian Sea basin.

Phylogeography and systematics of zebra mussels and related species.

The genus Dreissena includes two widespread and aggressive aquatic invaders, the zebra mussel, Dreissena polymorpha, and the quagga mussel, Dreissena bugensis. This genus evolved in the Ponto‐Caspian Sea basin, characterized by dynamic instability over multiple timescales and a unique evolutionary environment that may predispose to invasiveness. The objectives of this study were to gain insights into the demographic history of Dreissena species in their endemic range, to reconstruct intraspecific phylogeographic relationships among populations, and to clarify systematics of the genus, using DNA sequences from the mitochondrial cytochrome oxidase I (COI) gene. We found four deeply diverged clades within this genus, with a basal split that approximately coincided with the Cretaceous–Tertiary boundary. Divergence events within the four base clades were much more recent, corresponding to geographically disjunct sets of populations, which might represent species complexes. Across all taxa, populations of Dreissena shared a common pattern of genetic signatures indicating historical population bottlenecks and expansions. Haplotype diversity was relatively low in Ponto‐Caspian drainages relative to more stable tectonic lakes in Greece, Macedonia, and Turkey. The phylogeographic and demographic patterns in the endemic range of Dreissena might have resulted from vicariance events, habitat instability, and the high fecundity and passive dispersal of these organisms.

Testing for beneficial reversal of dominance during salinity shifts in the invasive copepod Eurytemora affinis, and implications for the maintenance of genetic variation.

Maintenance of genetic variation at loci under selection has profound implications for adaptation under environmental change. In temporally and spatially varying habitats, non‐neutral polymorphism could be maintained by heterozygote advantage across environments (marginal overdominance), which could be greatly increased by beneficial reversal of dominance across conditions. We tested for reversal of dominance and marginal overdominance in salinity tolerance in the saltwater‐to‐freshwater invading copepod Eurytemora affinis. We compared survival of F1 offspring generated by crossing saline and freshwater inbred lines (between‐salinity F1 crosses) relative to within‐salinity F1 crosses, across three salinities. We found evidence for both beneficial reversal of dominance and marginal overdominance in salinity tolerance. In support of reversal of dominance, survival of between‐salinity F1 crosses was not different from that of freshwater F1 crosses under freshwater conditions and saltwater F1 crosses under saltwater conditions. In support of marginal overdominance, between‐salinity F1 crosses exhibited significantly higher survival across salinities relative to both freshwater and saltwater F1 crosses. Our study provides a rare empirical example of complete beneficial reversal of dominance associated with environmental change. This mechanism might be crucial for maintaining genetic variation in salinity tolerance in E. affinis populations, allowing rapid adaptation to salinity changes during habitat invasions.

Direct sequencing of haplotypes from diploid individuals through a modified emulsion PCR-based single-molecule sequencing approach

While standard DNA‐sequencing approaches readily yield genotypic sequence data, haplotype information is often of greater utility for population genetic analyses. However, obtaining individual haplotype sequences can be costly and time‐consuming and sometimes requires statistical reconstruction approaches that are subject to bias and error. Advancements have recently been made in determining individual chromosomal sequences in large‐scale genomic studies, yet few options exist for obtaining this information from large numbers of highly polymorphic individuals in a cost‐effective manner. As a solution, we developed a simple PCR‐based method for obtaining sequence information from individual DNA strands using standard laboratory equipment. The method employs a water‐in‐oil emulsion to separate the PCR mixture into thousands of individual microreactors. PCR within these small vesicles results in amplification from only a single starting DNA template molecule and thus a single haplotype. We improved upon previous approaches by including SYBR Green I and a melted agarose solution in the PCR, allowing easy identification and separation of individually amplified DNA molecules. We demonstrate the use of this method on a highly polymorphic estuarine population of the copepod Eurytemora affinis for which current molecular and computational methods for haplotype determination have been inadequate.