Kyle W. Wellband

Novel molecular approach demonstrates that turbid river plumes reduce predation mortality on larval fish

Turbidity associated with river plumes is known to affect the search ability of visual predators and thus can drive ‘top‐down’ impacts on prey populations in complex ecosystems; however, traditional quantification of predator–prey relationships (i.e. stomach content analysis) often fails with larval fish due to rapid digestion rates. Herein, we use novel molecular genetic methods to quantify larval yellow perch (YP) in predator stomachs in western Lake Erie to test the hypothesis that turbidity drives variation in larval predation. We characterize predator stomach content DNA to first identify YP DNA (single nucleotide polymorphism) and then quantify larval YP predation (microsatellite allele counting) in two river plumes differing in turbidity. Our results showed elevated larval YP predation in the less turbid river plume, consistent with a top‐down impact of turbidity on larval survival. Our analyses highlight novel ecological hypothesis testing using the power of innovative molecular genetic approaches.

Plasticity in gene transcription explains the differential performance of two invasive fish species

Phenotypic plasticity buffers organisms from environmental change and is hypothesized to aid the initial establishment of nonindigenous species in novel environments and postestablishment range expansion. The genetic mechanisms that underpin phenotypically plastic traits are generally poorly characterized; however, there is strong evidence that modulation of gene transcription is an important component of these responses. Here, we use RNA sequencing to examine the transcriptional basis of temperature tolerance for round and tubenose goby, two nonindigenous fish species that differ dramatically in the extent of their Great Lakes invasions despite similar invasion dates. We used generalized linear models of read count data to compare gene transcription responses of organisms exposed to increased and decreased water temperature from those at ambient conditions. We identify greater response in the magnitude of transcriptional changes for the more successful round goby compared with the less successful tubenose goby. Round goby transcriptional responses reflect alteration of biological function consistent with adaptive responses to maintain or regain homeostatic function in other species. In contrast, tubenose goby transcription patterns indicate a response to stressful conditions, but the pattern of change in biological functions does not match those expected for a return to homeostatic status. Transcriptional plasticity plays an important role in the acute thermal tolerance for these species; however, the impaired response to stress we demonstrate in the tubenose goby may contribute to their limited invasion success relative to the round goby. Transcriptional profiling allows the simultaneous assessment of the magnitude of transcriptional response as well as the biological functions involved in the response to environmental stress and is thus a valuable approach for evaluating invasion potential.

Fine-Scale Population Genetic Structure and Dispersal of Juvenile Steelhead in the Bulkley-Morice River, British Columbia

Abstract A knowledge of fine-scale population genetic structure and patterns of dispersal is an essential component of any action to conserve genetic diversity and maintain population viability. We genotyped 417 juvenile steelhead Oncorhynchus mykiss from the main stem and tributaries of the Bulkley–Morice River, British Columbia, at 10 microsatellite loci to assess fine-scale population structure and the patterns and magnitude of juvenile dispersal and mixing. We detected significant genetic structuring among juvenile steelhead from seven tributaries of the Bulkley–Morice River (pairwise F ST: 0.008–0.156) and found significant isolation by distance among the tributary populations (R 2 = 0.198, P = 0.038). These results reflect the homing behavior of spawning adults as well as the temporal stability of those populations. Genotype assignment of tributary-caught juveniles showed that rates of juvenile dispersal varied among tributaries. The assignment of juveniles sampled from the main stem of the river to...

Environmental associations with gene transcription in Babine Lake rainbow trout: evidence for local adaptation

The molecular genetic mechanisms facilitating local adaptation in salmonids continue to be poorly characterized. Gene transcription is a highly regulated step in the expression of a phenotype and it has been shown to respond to selection and thus may be one mechanism that facilitates the development of local adaptation. Advances in molecular genetic tools and an increased understanding of the functional roles of specific genes allow us to test hypotheses concerning the role of variable environments in shaping transcription at known-function candidate loci. To address these hypotheses, wild rainbow trout were collected in their first summer and subjected to metabolic and immune challenges. We assayed gene transcription at candidate loci that play a role in the molecular genetic response to these stresses, and correlated transcription with temperature data from the streams and the abundance and diversity of bacteria as characterized by massively parallel pyrosequencing. Patterns of transcriptional regulation from resting to induced levels varied among populations for both treatments. Co-inertia analysis demonstrated significant associations between resting levels of metabolic gene transcription and thermal regime (R2 = 0.19, P = 0.013) as well as in response to challenge (R2 = 0.39, P = 0.001) and resting state and challenged levels of cytokine gene transcription with relative abundances of bacteria (resting: R2 = 0.25, P = 0.009, challenged: R2 = 0.65, P = 0.001). These results show that variable environments, even within a small geographic range (<250 km), can drive divergent selection among populations for transcription of genes related to surviving stress.

Differential invasion success in aquatic invasive species: the role of within- and among-population genetic diversity

Despite a well-developed theoretical basis for the role of genetic diversity in the colonization process, contemporary investigations of genetic diversity in biological invasions have downplayed its importance. Observed reductions in genetic diversity have been argued to have a limited effect on the success of establishment and impact based on empirical studies; however, those studies rarely include assessment of failed or comparatively less-successful biological invasions. We address this gap by comparing genetic diversity at microsatellite loci for taxonomically and geographically paired aquatic invasive species. Our four species pairs contain one highly successful and one less-successful invasive species (Gobies: Neogobius melanostomus, Proterorhinus semilunaris; waterfleas: Bythotrephes longimanus, Cercopagis pengoi; oysters: Crassostrea gigas, Crassostrea virginica; tunicates: Bortylloides violaceous, Botryllus schlosseri). We genotyped 2717 individuals across all species from multiple locations in multiple years and explicitly test whether genetic diversity is lower for less-successful biological invaders within each species pair. We demonstrate that, for gobies and tunicates, reduced allelic diversity is associated with lower success of invasion. We also found that less-successful invasive species tend to have greater divergence among populations. This suggests that intraspecific hybridization may be acting to convert among-population variation to within-population variation for highly successful invasive species and buffering any loss of diversity. While our findings highlight the species-specific nature of the effects of genetic diversity on invasion success, they do support the use of genetic diversity information in the management of current species invasions and in the risk assessment of potential future invaders.

The relative contribution of drift and selection to transcriptional divergence among Babine Lake tributary populations of juvenile rainbow trout

Fine‐scale population structure has been widely described for salmonid populations using neutral genetic markers, but whether that structure reflects adaptive differences among the populations remains of interest to evolutionary biologists and conservation managers alike. The use of transcriptomics to quantify population differences in genetically controlled functional gene expression traits holds promise for investigating this divergence associated with possible local adaptation. We use custom microarrays to characterize population divergence in transcription at functionally relevant (metabolic and immune function) genes among tributary populations of rainbow trout from Babine Lake, BC and compare it to neutral divergence estimated from microsatellite markers. Transcriptional divergence (PST) was determined at resting state and in response to metabolic and immune challenges, two major sources of mortality and thus selective forces on juvenile salmonids. Results indicate that the majority of selected genes [56 genes (65%), 64 genes (63%) and 38 genes (78%) under control, temperature and immune challenges respectively] show transcriptional divergence (PST > FST) that is consistent with the action of divergent selection. Patterns of pairwise PST among populations are inconsistent with evolution by drift. In general, it appears that the magnitude and pattern of population divergence in transcription reflect the action of natural selection and identify selection on transcription as a mechanism for local adaptation. These results reinforce the need to conserve salmonids on a tributary basis and provide insight into genetic mechanisms that facilitate local adaptation.

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 gobys 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.

Environmental and genetic determinants of transcriptional plasticity in Chinook salmon

Variation in gene transcription is widely believed to be the mechanistic basis of phenotypically plastic traits; however, comparatively little is known about the inheritance patterns of transcriptional variation that would allow us to predict its response to selection. In addition, acclimation to different environmental conditions influences acute transcriptional responses to stress and it is unclear if these effects are heritable. To address these gaps in knowledge, we assayed levels of messenger RNA for 14 candidate genes at rest and in response to a 24-h confinement stress for 72 half-sib families of Chinook salmon reared in two different environments (hatchery and semi-natural stream channel). We observed extensive plasticity for mRNA levels of metabolic and stress response genes and demonstrated that mRNA level plasticity due to rearing environment affects mRNA level plasticity in response to stress. These effects have important implications for natural populations experiencing multiple stressors. We identified genotype-by-environment interactions for mRNA levels that were dominated by maternal effects; however, mRNA level response to challenge also exhibited a non-additive genetic basis. Our results indicate that while plasticity for mRNA levels can evolve, predicting the outcome of selection will be difficult. The inconsistency in genetic architecture among treatment groups suggests there is considerable cryptic genetic variation for gene expression.

Human-mediated and natural dispersal of an invasive fish in the eastern Great Lakes

The globally invasive Round Goby (Neogobius melanostomus) was introduced to the Great Lakes around 1990, spreading widely and becoming the dominant benthic fish in many areas. The speed and scope of this invasion is remarkable and calls into question conventional secondary spread models and scenarios. We utilized nine microsatellites to identify large-scale genetic structure in Round Goby populations in the eastern Great Lakes, and assessed the role of colonization vs. secondary transport and dispersal in developing this structure. We identified three clusters, corresponding with Lake Huron, eastern Lake Erie, and western Lake Erie plus eastern Lake Ontario, along with three highly divergent populations. Bottleneck analysis identified founder effects in two divergent populations. Regression analyses of isolation by distance and allelic richness vs. distance from the initial invasion site were consistent with limited migration. However, some populations in eastern Lake Erie and Lake Ontario showed anomalously low genetic distance from the original site of colonization, consistent with secondary transport of large numbers of individuals via ballast water. We conclude that genetic structure of Round Goby in the Great Lakes principally resulted from long-distance secondary transport via ballast water with additional movement of individual via bait buckets and natural dispersal. The success of Round Gobies represents an interesting model for colonization characterization; however, those same attributes present significant challenges for conservation and fisheries management. Current management likely prevents many new species from arriving in the Great Lakes, but fails to address the transport of species within the lakes after they arrive; this is an issue of clear and pressing importance.