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Genetics of speciation in sympatric char; population genomics; conservation
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Graduate Student Supervision
Doctoral Student Supervision (Jan 2008 - May 2021)
Temperature influences biological processes at all levels of biological organization. As such, temperature is a fundamental abiotic variable affecting ectotherm fitness. As human induced climate change persists, the need to understand biological responses to temperature has never been more pressing. One consequence of rapid climate change is an increase in the frequency and intensity of heat waves. Despite substantial interest in the physiological effects of heat stress, it is less clear how individual responses to extreme heat events influence population-level responses such as persistence and population growth. Energy balance is a unifying concept that integrates the effect of temperature across scales. The Energy Limited Tolerance to Stress (ELTOS) framework links physiological models of temperature and oxygen availability to dynamic energy budgets in order to predict the effect of stress on individual reproduction and population growth. Drawing on the ELTOS framework, I tested three critical predictions about individual thermal experience, and how the influence of heat stress scales up from physiological to individual to populations, utilizing the splash pool copepod, Tigriopus californicus. In Chapter 2, I tested the prediction that aerobic energy production declines with increasing heat wave intensity and duration, and that individual reproduction declines similarly. In Chapter 3, I tested the assumption that short-term impacts of heat waves on individual reproduction have persistent effects on longer-term population dynamics. In Chapter 4, I tested for an effect of spatial variation in thermal history on subsequent heat wave survival. Together, these tests provide a comprehensive examination of ELTOS predictions of biological responses to heat waves across scales. My data are consistent with ELTOS predictions that heat wave intensity affects energy balance and subsequent individual reproductive effort. However, I did not find consistent patterns of population dynamics over both short and longer-term time scales. The opposing effect of temperature on different life-history traits that occur over different time-scales likely underlies differences in the effect of short-term heat wave effects on population dynamics over short and longer time periods. Lastly, I found that spatial variation in thermal history, particularly recent heat accumulation, explains reduced survivorship during experimental heat waves.
Dispersal can have a multitude of ecological and evolutionary consequences that can be either positive or negative for population fitness and persistence. In this thesis, I describe patterns of dispersal in Arctic Char (Salvelinus alpinus), and I explored some of its consequences. I first examined the consequences of post-glacial dispersal for the distribution of genetic variation across the Canadian range of the species. MtDNA sequences and microsatellite markers provided evidence that the populations of Arctic Char currently inhabiting the Arctic Archipelago probably recolonized from a small glacial refugium, most likely located in ice-free areas of the Archipelago itself. I also presented evidence that two glacial lineages of Char (an Arctic lineage and an Atlantic lineage) probably hybridized post-glacially in the eastern Arctic. Finally, the importance of contemporary dispersal in redistributing genetic variation was illustrated by the fact that anadromous populations have greater within-population genetic diversity, and are less genetically differentiated, than landlocked populations. Second, I used a genetic assignment approach to study patterns of dispersal among populations distributed around Cumberland Sound, Nunavut. Estimates of dispersal rates varied extensively depending on the analysis method used, but all were relatively high compared to other salmonid species. I also found evidence that overwintering individuals have a greater propensity to disperse to non-natal habitats than individuals destined to spawn that year. The consequences of this behaviour for local adaptation among populations was examined using a population genetic model parameterized with estimates of gene flow obtained from microsatellite data. Third, I tested alternative hypotheses for the co-existence of sympatric migratory ecotypes in three lakes of southeast Baffin Island. Microsatellite data showed that the resident and anadromous components of the population are not genetically differentiated, suggesting that migratory behavior is not a genetically fixed trait. Together, the three parts of my thesis provide a general understanding of the patterns and consequences of dispersal for Arctic Char. Since dispersal will be crucial for the response of Arctic Char to environmental change, I conclude by discussing how my work can serve as a foundation for future work on the role of dispersal in adaptation to a changing Arctic.
In sperm-dependent asexual reproduction, sperm is not required for its genetic contribution, but it is required for stimulating zygote development. In my dissertation, I address several questions related to the coexistence of sperm-dependent asexuals and the sexually-reproducing species on which they depend. I have focused my research on a sperm-dependent asexual fish, Phoxinus eos-neogaeus, that originated via hybridization between P. eos and P. neogaeus.Using a mathematical model of mate choice among sexuals and sperm-dependent asexuals, I showed that stable coexistence can occur when there is variation among males in the strength of preference for mating with sexual females and when males with stronger preference pay a higher cost of preference. My model also predicts that coexistence is facilitated when the asexuals suffer a fitness disadvantage relative to the sexuals. Subsequent empirical work, in which I compared the repeat swimming performance, fecundity, and growth rate of asexual and sexual Phoxinus, provided results that are consistent with this prediction: the asexuals are, at best, as fit as the sexuals.I sampled Phoxinus populations from across the species’ North American distribution and the pattern of mitochondrial DNA variation across these populations suggests that all P. eos-neogaeus have originated from hybridization events that took place in a Mississippi River glacial refugium. Also, cytoplasmic hybrids (which are P. eos with P. neogaeus mitochondrial DNA) appear to have replaced ‘pure’ P. eos in all northern populations, which may reduce the disparity in fitness between P. eos-neogaeus and their sperm donors if P. neogaeus mitochondria are adapted to northern environments. The pattern of nuclear DNA variation across P. eos-neogaeus populations suggests that those using P. eos sperm are genetically distinct from those using P. neogaeus sperm. These genetically distinct populations match their host species in size, suggesting that sperm-dependent asexuals may be adapted to be proficient at soliciting sperm from particular sexual species.Persistence of sperm-dependent asexuals depends on stable coexistence with sexual species. My work highlights the importance of the relative fitness of asexual and sexual species, and of male mate choice in maintaining this stable coexistence.
Master's Student Supervision (2010 - 2020)
The Salish sucker (Catostomus sp. cf. catostomus) is a federally Threatened species under Canada’s Species at Risk Act and is restricted to 11 watersheds in British Columbia (lower Fraser River Valley) and six in Washington State. Agricultural development has been historically prominent in these areas, and hypoxia and the physical destruction of habitat have been identified as the most important threats to this species. Synergistic effects of reduced streamflow, nutrient inputs, and high temperatures are likely large determinants of seasonal hypoxia. The effects of stream flow on temperature and dissolved oxygen in Salish sucker critical habitat, and corresponding changes in habitat use, distribution, and growth of Salish sucker were studied. As salmonids are even more sensitive to impaired water quality than suckers, and maintaining salmonid populations is an additional major conservation concern in the lower Fraser Valley, the biological response of juvenile coho salmon was also studied as they co-occur in Salish sucker habitats. Through various flow manipulation and enclosure experiments I found that severely reducing flow in off-channel ponds resulted in low levels of dissolved oxygen (
This research investigated a population of lake chub (Couesius plumbeus) inhabiting a geothermal spring complex south of the community of Atlin, in the far northwest of British Columbia. These lake chub live in thermal isolation in 13-26°C water year round, while the only neighbouring water body, glacier-fed Atlin Lake, remains below 6°C year round and has no known population of lake chub. Through mark-recapture sampling I estimated the population size of this isolated and physiologically distinct population to be on the order of 1,000 to 2,000 mature individuals. I measured its area of occupancy as 3,602m². As such, the population is small in both habitat extent and population size, as well as being physically isolated from other populations of this widespread species. Tagging of fish in individual sections of the warm springs showed a general lack of movement among different sites. Size-frequency histograms for individual sites and points in time illustrated the presence of distinct cohorts suggesting lifespans of three to four years, with outliers living a year or two longer. I also studied the invasive cherry shrimp (Neocaridina davidi var. red), performing experiments to observe survivorship and behaviour under different temperature regimes. I found no significant decrease in mortality in adults when water was cooled to 5°C, but a significant reduction in their ability to react to stimuli below 15°C. I also observed 100% mortality in juveniles at water temperatures of 10°C or lower within two days. Based on these data, barring future adaptation to considerably colder conditions, is unlikely that cherry shrimp will be able to expand their range further into the Yukon River basin. Overall, my study provides a baseline of understanding about the population and life history of an isolated warm-springs population of lake chub, and provides observations of the early stages and probable outcomes of an exotic species invading an isolated location.
Resource polymorphism and natural hybridization are evolutionary phenomena that play an important role in the development of reproductive isolation during speciation. The Arctic char (Salmonidae: Salvelinus alpinus) exhibits substantial phenotypic and genetic diversity across its Holarctic range, making it an ideal species to examine the role of intraspecific trophic polymorphism in driving reproductive isolation and the interactions between hybridizing species in sympatry. In one southwestern post-glacial lake previously analyzed for resource polymorphism (Lower Tazimina Lake), I found evidence for two genetic groups of char and for significant differences in the distribution of microsatellite variability among at least two of the three previously described body-size morphotypes (‘large’, ‘medium’, and ‘small’–bodied char; maximum FST = 0.09). I also found significant associations between genetic type and gill raker counts among body-size morphs (r = -0.73, P
Natural selection and local adaptation influence fish abundances and distributions on both short and long-term time scales: first, by influencing recruitment dynamics and second, by affecting long-term population persistence in fluctuating environmental conditions. Little is known, however, about the significance of adaptive population divergence in the marine environment. In this study, I utilized an FST outlier approach to detect putatively selected loci from an Amplified Fragment Length Polymorphism (AFLP) marker dataset of yelloweye rockfish (Sebastes ruberrimus) collected from southeast Alaska south to Oregon. During the data analysis phase, a plate bias was detected and efforts to eliminate this effect were unsuccessful. Therefore, each PCR plate was analyzed separately, resulting in seven independent analyses. A total of 966-1580 AFLP loci were identified for the seven plates, and 0-10 loci (0-0.79%) per plate were identified as FST outliers by program, BAYESCAN. Based on results from the outlier analyses, datasets composed of neutral loci (those with no support for being under selection) and outlier loci (those exceeding a minimum posterior threshold of 0.7, corresponding to a moderate amount of support for being under selection) were established for each plate. Global FST values are approximately five times greater for the outlier datasets (mean FST=0.56) than for putatively neutral loci (mean FST=0.10). The genetic clustering program, STRUCTURE, identified similar patterns of population structure both for the neutral and outlier datasets. The outlier datasets, however, lead to overall higher assignment probabilities of individual fish to genetic groups than observed with the neutral datasets. In addition, several similar clustering patterns (e.g. southern vs. northern genetic clusters, presence of isolated clusters) were observed across several plates, providing independent evidence for regionally restricted gene flow. Overall, my results suggest that population structure driven by neutral processes may be reinforced by natural selection, which has implications for the management of yelloweye rockfish fishery stocks and the scale of connectivity within the Rockfish Conservation Area marine reserve network.
Brassy minnow, Hybognathus hankinsoni, is a little-studied cyprinid fish with highly disjunct distributions in western Canada. Phylogeographic scenarios on the origins of brassy minnow in British Columbia (BC) were explored using two mitochondrial loci (cyt b and ND4) that were sequenced for up to 32 localities. This revealed an approximate ‘east-west’ geographic split, suggesting that BC populations are likely post-glacial colonists from the Mississippi-Missouri refugium. However, certain ‘eastern’ populations exhibited incongruences between gene and species trees, suggesting complex evolutionary histories in brassy minnow. Sampling brassy minnow within BC revealed highest catch rates in the Interior of the province, and a year-long survey conducted in the Lower Mainland (n = 60 sites), revealed that brassy minnow abundances were highest at Westham Island. A logistic-regression habitat model was performed incorporating seven physical habitat parameters over 37 sites, identifying conductivity as a near significant parameter for predicting brassy minnow presence. Additionally, in the Lower Mainland, eight invasive species constituted 28 % of the relative abundance of species sampled. Compared to historical records from the University of BC Fish Museum, sites exhibited a significant decline in the number of cypriniform species, including brassy minnow, but showed no significant change in the number of invasive species present. A detrended correspondence analysis (DCA) of species abundance across sites suggested brassy minnow overlapped most closely with two invasive species: bullfrogs, Lithobates catesbieanus, and brown bullhead, Ameiurus nebulosus. To explore the impact of brown bullhead on brassy minnow, pools with and without adult brown bullhead were compared at Tamboline Slough, Westham Island, and showed significant differences in the native fish species abundances across pools, including brassy minnow. Additionally, growth experiments were conducted over 90 days with brassy minnow, young-of-year brown bullhead, and redside shiner, Richardsonius balteatus, kept in all possible combinations for a total of four treatments per species. Treatments showed that brassy minnow were the only species to exhibit weight loss and mortality when with other species. In addition to providing insights into the biogeography, ecology, and conservation implications of brassy minnow, my thesis provides a quantitative baseline for invasive species found within the Lower Mainland.
The Cultus pygmy sculpin (Cottus aleuticus) is endemic to Cultus Lake, southwestern BC, and is listed as threatened under the federal Species at Risk Act (SARA). The Cultus pygmy sculpin was first discovered by Ricker in the 1930’s (Ricker 1960) and was described as a dwarf coastrange sculpin (C. aleuticus). It matures at a smaller size than the “normal” C. aleuticus; has a lacustrine rather than a fluvial life history; and appears to undertake diurnal feeding migrations into the water column to feed on the abundance of Daphnia. The Cultus pygmy sculpin also has different morphological features, including larger cephalic pores, shorter pelvic fins, and a greater number of pectoral fin rays, which may be advantageous for an open-water, planktivorous lifestyle. Little else, however, is known of the biology of this fish. I used mtDNA and microsatellite analyses to determine whether there is any genetic distinction between the pygmy sculpin and the coastrange sculpin. Potential behavioural differences between the two forms were also examined by comparing vertical depth selection in the laboratory, with and without Cottus asper, a benthic predator found in Cultus Lake. Results from combined microsatellite and mtDNA analyses indicate that there is no clear phylogeographic separation between pygmy and coastrange sculpin, but that there is genetic differentiation at the population level. Pelagic sculpin from Lake Washington were compared with the Cultus pygmy sculpin and showed divergence from it, which suggests that the pelagic life history has evolved independently in each lake. The Cultus pygmy sculpin was found significantly higher in experimental depth selection tanks than the stream forms of C. aleuticus, but only when C. asper was also present in the tanks. Taken together, molecular and behavioural results indicate that the Cultus pygmy sculpin is discrete from the coastrange sculpin, and validate its recognition as a conservation unit distinct from “typical” C.aleuticus. The presence of abundant planktonic prey within the water column of Cultus Lake, combined with the presence of predators on the lake’s bottom, may be important features of the lake that have promoted the evolution of pelagic behaviour by the Cultus pygmy sculpin.
Southwestern British Columbia is unique in that it is apparently the only place on Earth with sympatric species pairs of threespine stickleback (Gasterosteus aculeatus). As such, these species pairs are listed as endangered and are protected under Canada’s Species at Risk Act. Historically these species pairs inhabited seven known lakes but their distribution is currently limited to five lakes in three watersheds. Within these lakes stickleback are found in two forms: benthic and limnetic. These species pairs are thought to have originated through a double-invasion process followed by character displacement. While this hypothesis is supported by morphology and genetics it does not take into account the environmental factors needed to support threespine stickleback in two separate microhabitats, which may be essential for their continued persistence. It is conceivable that the divergence and persistence of the threespine stickleback species pairs may be due in part to unique environmental characteristics of the lakes they inhabit, including physical lake characteristics, water chemistry, or biological productivity. Alternatively, divergence and persistence could be due to specific attributes of fish community structure or random colonization events unrelated to lake attributes. To establish this, I measured a number of abiotic (water chemistry, physical lake parameters) and biotic (food resources, macrophyte abundance) variables from both species pair and non-species pair threespine stickleback lakes in order to identify any factors that may discriminate species pair lakes from non-species pair lakes, thereby leading to a clearer understanding of their critical habitat. While I did not find any clear environmental differences between species pair and non-species pair lakes, my study suggests that a major determinant of the existence of stickleback species pairs is the community of fish present in the lakes and that nesting habitat heterogeneity and its influence on pre-mating reproductive barriers may be important to the persistence of these species pairs. My study provides a baseline to monitor the environments for all known species pair lakes and suggests that the fish assemblage in stickleback lakes may affect resource availability as strongly as the limnological attributes of the lakes themselves although predation may also be an important factor in the evolution of these species pairs.
Biodiversity is of critical importance to the quality of life on Earth. In light of rapidly increasing extinction rates in recent years, understanding threats to biodiversity such as habitat destruction, over-exploitation, and the introduction of invasive species is of utmost importance to conservation efforts. Invasive species, in particular, are a threat of great concern in aquatic environments, due, in part, to their potential role in facilitating introgressive hybridization between closely related species. In recent decades, such a case of hybridization has led to genomic extinction in a benthic-limnetic species pair of threespine stickleback (Gasterosteus aculeatus) in Enos Lake, British Columbia, following the appearance of invasive American signal crayfish (Pacifastacus leniusculus) in this waterbody. In an effort to shed light on the potential role of these crayfish in this loss of diversity, research was conducted using an intact species pair from Paxton Lake, BC to determine if crayfish exert meaningful impacts on sticklebacks through the disruption of i) male stickleback reproductive behaviours and/or ii) juvenile stickleback growth rates. The results of reproductive behaviour trials demonstrated that limnetic male reproductive behaviour frequency was suppressed to a greater degree than that of benthic males in the presence of crayfish. This result suggests that crayfish disruptions may reduce conspecific mating opportunities for limnetic females, thus leading to increases in introgressive hybridization between benthic males and limnetic females. The results of the juvenile growth rate trial, on the other hand, demonstrated that crayfish do not disrupt growth rates of juveniles; however, significantly higher stickleback mortality levels were detected in the presence of crayfish. I conclude that invasive American signal crayfish have likely facilitated introgressive hybridization between the Enos Lake species pair, but other factors may have contributed to this loss of biodiversity. My study highlights the sensitivity of recently differentiated species to disruption by invasive species. By identifying important sources of ecological disruption and significant threats to biodiversity, such studies are critical for guiding conservation efforts in Canada and worldwide.