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Matthew C. Boyer

Publications and source records attributed to Matthew C. Boyer.

12 recordsLinked to original sources

Invasive hybridization has unpredicted and variable effects on trout survival in contrasting environments

Invasive hybridization between native and introduced species is widespread, especially in fishes, yet its effects on fitness-related traits across environments remain poorly understood. We combined individual genetic admixture estimates with capture–recapture data to quantify how hybridization between native Westslope Cutthroat Trout ( Oncorhynchus lewisi ) and invasive Rainbow Trout ( Oncorhynchus mykiss ) influences survival. We measured individual survival of 5186 trout across three populations in contrasting environments. Non-native admixture significantly affected survival in two populations, with positive effects during summer and negative effects during winter. Prior research has shown hybridization increases with stream temperature; however, survival patterns did not follow this trend. In a warmer stream, native trout in all size-classes had ≥20% higher annual survival than hybrids, whereas in a cooler stream, juvenile native trout had ≥20% lower survival than hybrids. These findings indicate that hybridization effects on survival are complex and vary among populations, environments, and size-classes. Landscape patterns of hybridization may therefore not reflect local survival (or fitness) outcomes, emphasizing that measures fitness-related traits across populations and environments could elucidate the eco-evolutionary consequences of invasive hybridization.

Canadian Journal of Fisheries and Aquatic Sciences

Rapid SNP genotyping, sex identification, and hybrid-detection in threatened bull trout

We developed new bull trout genetic markers using Restriction-site Associated DNA sequencing (RAD-seq) to improve our ability to address questions important for their conservation and management. Samples from across the species range were sequenced and 5020 high quality single nucleotide polymorphism (SNP) loci were discovered, including hundreds with high heterozygosity ( H > 0.30). We developed 63 high-heterozygosity bull trout polymorphic SNPs and one sex-identification SNP and tested them on range-wide samples. In addition, we tested previously published SNP assays including 11 species-diagnostic SNPs differentiating bull trout from brook trout and 3 brook trout variable SNPs on a broad set of range-wide samples. Genotypes from the sex-identification SNP showed 95% agreement with the field sex identification across 113 samples. The eleven species-diagnostic loci reliably discriminated between known brook trout, bull trout, and F 1 hybrid control samples. These SNP assays will facilitate genotyping of partially degraded museum fin clips, and tissues with low DNA content such as scales and otoliths. Finally, these loci will allow rapid genotyping for improved resolution of bull trout population structure, sex ratios, movement patterns, and introgressive hybridization with non-native brook trout for a wide range of management questions.

British Columbia, Idaho, Montana, Nevada, Oregon,

Detecting population declines via monitoring the effective number of breeders (Nb)

Estimating the effective population size and effective number of breeders per year ( N b ) can facilitate early detection of population declines. We used computer simulations to quantify bias and precision of the one-sample LDNe estimator of N b in age-structured populations using a range of published species life history types, sample sizes, and DNA markers. N b estimates were biased by ~5%–10% when using SNPs or microsatellites in species ranging from fishes to mosquitoes, frogs, and seaweed. The bias (high or low) was similar for different life history types within a species suggesting that life history variation in populations will not influence N b estimation. Precision was higher for 100 SNPs ( H ≈ 0.30) than for 15 microsatellites ( H ≈ 0.70). Confidence intervals (CIs) were occasionally too narrow, and biased high when N b was small ( N b < 50); however, the magnitude of bias would unlikely influence management decisions. The CIs (from LDNe ) were sufficiently narrow to achieve high statistical power (≥0.80) to reject the null hypothesis that N b = 50 when the true N b = 30 and when sampling 50 individuals and 200 SNPs. Similarly, CIs were sufficiently narrow to reject N b = 500 when the true N b = 400 and when sampling 200 individuals and 5,000 loci. Finally, we present a linear regression method that provides high power to detect a decline in N b when sampling at least five consecutive cohorts. This study provides guidelines and tools to simulate and estimate N b for age structured populations ( https://github.com/popgengui/agestrucnb/ ), which should help biologists develop sensitive monitoring programmes for early detection of changes in N b and population declines.

Molecular Ecology Resources

Hybridization alters growth and migratory life-history expression of native trout

Human-mediated hybridization threatens many native species, but the effects of introgressive hybridization on life-history expression are rarely quantified, especially in vertebrates. We quantified the effects of non-native rainbow trout admixture on important life-history traits including growth and partial migration behavior in three populations of westslope cutthroat trout over five years. Rainbow trout admixture was associated with increased summer growth rates in all populations and decreased spring growth rates in two populations with cooler spring temperatures. These results indicate that non-native admixture may increase growth under warmer conditions, but cutthroat trout have higher growth rates during cooler periods. Non-native admixture consistently increased expression of migratory behavior, suggesting that there is a genomic basis for life-history differences between these species. Our results show that effects of interspecific hybridization on fitness traits can be the product of genotype-by-environment interactions even when there are minor differences in environmental optima between hybridizing species. These results also indicate that while environmentally mediated traits like growth may play a role in population-level consequences of admixture, strong genetic influences on migratory life-history differences between these species likely explains the continued spread of non-native hybridization at the landscape-level, despite selection against hybrids at the population-level.

Montana

Vive la résistance: genome-wide selection against introduced alleles in invasive hybrid zones

Evolutionary and ecological consequences of hybridization between native and invasive species are notoriously complicated because patterns of selection acting on non-native alleles can vary throughout the genome and across environments. Rapid advances in genomics now make it feasible to assess locus-specific and genome-wide patterns of natural selection acting on invasive introgression within and among natural populations occupying diverse environments. We quantified genome-wide patterns of admixture across multiple independent hybrid zones of native westslope cutthroat trout and invasive rainbow trout, the world's most widely introduced fish, by genotyping 339 individuals from 21 populations using 9380 species-diagnostic loci. A significantly greater proportion of the genome appeared to be under selection favouring native cutthroat trout (rather than rainbow trout), and this pattern was pervasive across the genome (detected on most chromosomes). Furthermore, selection against invasive alleles was consistent across populations and environments, even in those where rainbow trout were predicted to have a selective advantage (warm environments). These data corroborate field studies showing that hybrids between these species have lower fitness than the native taxa, and show that these fitness differences are due to selection favouring many native genes distributed widely throughout the genome.

Proceedings of the Royal Society B: Biological Sci

Genetic status and conservation of Westslope Cutthroat Trout in Glacier National Park

Invasive hybridization is one of the greatest threats to the persistence of Westslope Cutthroat Trout Oncorhynchus clarkii lewisi . Large protected areas, where nonhybridized populations are interconnected and express historical life history and genetic diversity, provide some of the last ecological and evolutionary strongholds for conserving this species. Here, we describe the genetic status and distribution of Westslope Cutthroat Trout throughout Glacier National Park, Montana. Admixture between Westslope Cutthroat Trout and introduced Rainbow Trout O. mykiss and Yellowstone Cutthroat Trout O. clarkii bouvieri was estimated by genotyping 1,622 fish collected at 115 sites distributed throughout the Columbia, Missouri, and South Saskatchewan River drainages. Currently, Westslope Cutthroat Trout occupy an estimated 1,465 km of stream habitat and 45 lakes (9,218 ha) in Glacier National Park. There was no evidence of introgression in samples from 32 sites along 587 km of stream length (40% of the stream kilometers currently occupied) and 17 lakes (2,555 ha; 46% of the lake area currently occupied). However, nearly all (97%) of the streams and lakes that were occupied by nonhybridized populations occurred in the Columbia River basin. Based on genetic status (nonnative genetic admixture ≤ 10%), 36 Westslope Cutthroat Trout populations occupying 821 km of stream and 5,482 ha of lakes were identified as “conservation populations.” Most of the conservation populations ( N = 27; 736 km of stream habitat) occurred in the Columbia River basin, whereas only a few geographically restricted populations were found in the South Saskatchewan River ( N = 7; 55 km) and Missouri River ( N = 2; 30 km) basins. Westslope Cutthroat Trout appear to be at imminent risk of genomic extinction in the South Saskatchewan and Missouri River basins, whereas populations in the Columbia River basin are widely distributed and conservation efforts are actively addressing threats from hybridization and other stressors. A diverse set of pro-active management approaches will be required to conserve, protect, and restore Westslope Cutthroat Trout populations in Glacier National Park throughout the 21st century.

Glacier National Park

Risk and efficacy of human-enabled interspecific hybridization for climate-change adaptation: Response to Hamilton and Miller (2016)

Hamilton and Miller ( 2016 ) provide an interesting and provocative discussion of how hybridization and introgression can promote evolutionary potential in the face of climate change. They argue that hybridization&mdash;mating between individuals from genetically distinct populations&mdash;can alleviate inbreeding depression and promote adaptive introgression and evolutionary rescue. We agree that deliberate intraspecific hybridization (mating between individuals of the same species) is an underused management tool for increasing fitness in inbred populations (i.e., genetic rescue; Frankham 2015 ; Whiteley et al. 2015 ). The potential risks and benefits of assisted gene flow have been discussed in the literature, and an emerging consensus suggests that mating between populations isolated for approximately 50&ndash;100 generations can benefit fitness, often with a minor risk of outbreeding depression (Frankham et al. 2011 ; Aitken & Whitlock 2013 ; Allendorf et al. 2013 ).

Conservation Biology

Effects of hybridization between nonnative Rainbow Trout and native Westslope Cutthroat Trout on fitness-related traits

Hybridization between introduced and native fauna is a risk to native species and may threaten the long-term persistence of numerous taxa. Rainbow Trout Oncorhynchus mykiss has been one of the most widely introduced species around the globe and often hybridizes with native Cutthroat Trout O. clarkii in the Rocky Mountains. Previous work has shown that hybridization negatively affects reproductive success, but identification of the traits contributing to that reduction has been elusive. In this study, we used a combination of field and laboratory techniques to assess how hybridization with Rainbow Trout affects seven traits during several stages of Westslope Cutthroat Trout development: embryonic survival, ova size, ova energy concentration, sperm motility, juvenile weight, juvenile survival, and burst swimming endurance. Rainbow Trout admixture was correlated with an increase in embryonic survival and ova energy concentration but with a decrease in juvenile weight and burst swimming endurance. These correlations differed from previously observed patterns of reproductive success and likely do not explain the declines in reproductive success associated with admixture. Future investigation of additional, unstudied traits and the use of different environments may shed light on the traits responsible for reproductive success in admixed Cutthroat Trout.

Transactions of the American Fisheries Society

Dispersal and selection mediate hybridization between a native and invasive species

Hybridization between native and non-native species has serious biological consequences, but our understanding of how dispersal and selection interact to influence invasive hybridization is limited. Here, we document the spread of genetic introgression between a native (Oncorhynchus clarkii) and invasive (Oncorhynchus mykiss) trout, and identify the mechanisms influencing genetic admixture. In two populations inhabiting contrasting environments, non-native admixture increased rapidly from 1984 to 2007 and was driven by surprisingly consistent processes. Individual admixture was related to two phenotypic traits associated with fitness: size at spawning and age of juvenile emigration. Fish with higher non-native admixture were larger and tended to emigrate at a younger age&mdash;relationships that are expected to confer fitness advantages to hybrid individuals. However, strong selection against non-native admixture was evident across streams and cohorts (mean selection coefficient against genotypes with non-native alleles (s) &frac14; 0.60; s.e. &frac14; 0.10). Nevertheless, hybridization was promoted in both streams by the continuous immigration of individuals with high levels of non-native admixture from other hybrid source populations. Thus, antagonistic relationships between dispersal and selection are mediating invasive hybridization between these fish, emphasizing that data on dispersal and natural selection are needed to fully understand the dynamics of introgression between native and non-native species. .

Proceedings of the Royal Society B

Invasive hybridization in a threatened species is accelerated by climate change

Climate change will decrease worldwide biodiversity through a number of potential pathways 1 , including invasive hybridization 2 (cross-breeding between invasive and native species). How climate warming influences the spread of hybridization and loss of native genomes poses difficult ecological and evolutionary questions with little empirical information to guide conservation management decisions 3 . Here we combine long-term genetic monitoring data with high-resolution climate and stream temperature predictions to evaluate how recent climate warming has influenced the spatio-temporal spread of human-mediated hybridization between threatened native westslope cutthroat trout ( Oncorhynchus clarkii lewisi ) and non-native rainbow trout ( Oncorhynchus mykiss ), the world’s most widely introduced invasive fish 4 . Despite widespread release of millions of rainbow trout over the past century within the Flathead River system 5 , a large relatively pristine watershed in western North America, historical samples revealed that hybridization was prevalent only in one (source) population. During a subsequent 30-year period of accelerated warming, hybridization spread rapidly and was strongly linked to interactions between climatic drivers—precipitation and temperature—and distance to the source population. Specifically, decreases in spring precipitation and increases in summer stream temperature probably promoted upstream expansion of hybridization throughout the system. This study shows that rapid climate warming can exacerbate interactions between native and non-native species through invasive hybridization, which could spell genomic extinction for many species.

Alberta, Idaho, Montana

Quantifying the effectiveness of conservation measures to control the spread of anthropogenic hybridization in stream salmonids: A climate adaptation case study

Quantifying the effectiveness of management actions to mitigate the effects of changing climatic conditions (i.e., climate adaptation) can be difficult, yet critical for conservation. We used population genetic data from 1984 to 2011 to assess the degree to which ambient climatic conditions and targeted suppression of sources of nonnative Rainbow Trout Oncorhynchus mykiss have influenced the spread of introgressive hybridization in native populations of Westslope Cutthroat Trout O. clarkii lewisi . We found rapid expansion in the spatial distribution and proportion of nonnative genetic admixture in hybridized populations from 1984 to 2004, but minimal change since 2004. The spread of hybridization was negatively correlated with the number of streamflow events in May that exceeded the 75th percentile of historic flows ( r = −0.98) and positively correlated with August stream temperatures ( r = 0.89). Concomitantly, suppression data showed a 60% decline in catch per unit effort for fish with a high proportion of Rainbow Trout admixture, rendering some uncertainty as to the relative strength of factors controlling the spread of hybridization. Our results illustrate the importance of initiating management actions to mitigate the potential effects of climate change, even where data describing the effectiveness of such actions are initially limited but the risks are severe.

Montana

Genomic patterns of introgression in rainbow and westslope cutthroat trout illuminated by overlapping paired-end RAD sequencing

Rapid and inexpensive methods for genomewide single nucleotide polymorphism (SNP) discovery and genotyping are urgently needed for population management and conservation. In hybridized populations, genomic techniques that can identify and genotype thousands of species-diagnostic markers would allow precise estimates of population- and individual-level admixture as well as identification of 'super invasive' alleles, which show elevated rates of introgression above the genomewide background (likely due to natural selection). Techniques like restriction-site-associated DNA (RAD) sequencing can discover and genotype large numbers of SNPs, but they have been limited by the length of continuous sequence data they produce with Illumina short-read sequencing. We present a novel approach, overlapping paired-end RAD sequencing, to generate RAD contigs of >300–400 bp. These contigs provide sufficient flanking sequence for design of high-throughput SNP genotyping arrays and strict filtering to identify duplicate paralogous loci. We applied this approach in five populations of native westslope cutthroat trout that previously showed varying (low) levels of admixture from introduced rainbow trout (RBT). We produced 77 141 RAD contigs and used these data to filter and genotype 3180 previously identified species-diagnostic SNP loci. Our population-level and individual-level estimates of admixture were generally consistent with previous microsatellite-based estimates from the same individuals. However, we observed slightly lower admixture estimates from genomewide markers, which might result from natural selection against certain genome regions, different genomic locations for microsatellites vs. RAD-derived SNPs and/or sampling error from the small number of microsatellite loci (n = 7). We also identified candidate adaptive super invasive alleles from RBT that had excessively high admixture proportions in hybridized cutthroat trout populations.

Molecular Ecology