The role of phenotypic plasticity and genetic diversity in the colonization of novel environments

Phenotypic plasticity and genetic diversity are theorized to contribute to species’ successful colonization and range expansion; however, there is a lack of consensus in the invasion biology literature about their role in predicting invasion success. Much of the existing empirical research suffers from a lack of knowledge regarding failed or unsuccessful invasions. This reflects the scientific community’s priority for understanding the worst invaders. To address these gaps in knowledge, I used a novel comparative approach of taxonomically and geographically paired invasive species, representing successful and less-successful invaders, to investigate the potential of phenotypic plasticity for gene transcription and genetic diversity at both neutral and functional genetic markers to predict invasion success (Chapters 2, 4 and 5). I also addressed genetic and environmental underpinnings of phenotypic plasticity for gene transcription (Chapter 3) to improve the use of transcriptional variation to predict invasion success and range expansion. A highly successful biological invader was more transcriptionally plastic to temperature change, with a stronger transcriptional response and wider range of biological functions, than a comparatively less successful invader (Chapter 2). Transcriptional variation for core metabolic and stress response genes is primarily driven by the environment (Chapter 3) suggesting that, while transcription for potential invaders must be assayed under a range of conditions, knowledge of these responses will allow prediction of transcriptional profiles and thus an organism’s potential performance in, as yet, un-invaded areas. Low relative invasion success was associated with decreased levels of within- but elevated levels of among-population genetic diversity for two of four species pairs (Chapter 4). These results imply that genetic diversity is limiting for some invasive species’ range expansions and highlight the role that intraspecific hybridization may play in promoting invasion success. Compared to native range populations, tubenose goby have experienced a loss of genetic diversity while round goby have not. Round goby exhibit more adaptive divergence within the invaded range indicating that tubenose goby range expansion may be limited by its inability to evolve to facilitate range expansion (Chapter 5). Thus, both phenotypic plasticity and genetic diversity are important for successful range expansion and predicting colonization potential

Gene transcription mediated local adaptation of Babine Lake tributary rainbow trout

The adaptation of populations to their local environments has implications for speciation theory as well as the conservation and management of genetic diversity in those populations. The genetic mechanisms that underlie the process of local adaptation remain poorly characterized; however recent evidence suggests a role for the evolution of gene transcription regulation in the development of local adaptations. The goal of this thesis is to examine transcriptional divergence among genetically structured populations of juvenile rainbow trout from Babine Lake, BC and test the hypothesis that transcriptional divergence in this system reflects local adaptation. This thesis provides evidence that transcriptional divergence is present among Babine Lake tributaries, that gene transcription correlates with specific environmental parameters of tributaries and that patterns of divergence do not reflect a pattern of evolution by neutral drift. These results reinforce the need to conserve salmonid populations at fine spatial scales to preserve functional (transcriptional) genetic diversity

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

© 2017, Springer International Publishing AG Switzerland. 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

Data from: 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

Data from: 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 non-indigenous species in novel environments and post-establishment 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 non-indigenous 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 do 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

Data from: 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

R code for analysis of shared orthologs

This R code uses information about the reciprocal best BLAST matches between round and tubenose goby transcripts to combine and analyze the count datasets for shared orthologs

Unix shell script for transcriptome assembly and read mapping

This script was used to perform de novo transcriptome assembly and read mapping for both round and tubenose goby. Its inclusion is primarily to document specific parameters used for these analysis steps

Round goby transcript count data

This file was generated using Corset software to process BAM files of RNAseq reads mapped to a de novo assembled transcriptome for nine round goby and enumerate counts of reads per transcript as a proxy for transcript abundance