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1. Legacy introductions and climatic variation explain spatiotemporal patterns of invasive hybridization in a native trout

   https://doi.org/10.1111/gcb.13681  

   Muhlfeld, Clint C. ; Kovach, Ryan P. ; Al‐Chokhachy, Robert ; Amish, Stephen J. ; Kershner, Jeffrey L. ; Leary, Robb F. ; Lowe, Winsor H. ; Luikart, Gordon ; Matson, Phil ; Schmetterling, David A. ; et al ( April 2017 , Global Change Biology)

   Hybridization between invasive and native species, a significant threat to worldwide biodiversity, is predicted to increase due to climate‐induced expansions of invasive species. Long‐term research and monitoring are crucial for understanding the ecological and evolutionary processes that modulate the effects of invasive species. Using a large, multidecade genetics dataset (N = 582 sites, 12,878 individuals) with high‐resolution climate predictions and extensive stocking records, we evaluate the spatiotemporal dynamics of hybridization between native cutthroat trout and invasive rainbow trout, the world's most widely introduced invasive fish, across the Northern Rocky Mountains of the United States. Historical effects of stocking and contemporary patterns of climatic variation were strongly related to the spread of hybridization across space and time. The probability of occurrence, extent of, and temporal changes in hybridization increased at sites in close proximity to historical stocking locations with greater rainbow trout propagule pressure, warmer water temperatures, and lower spring precipitation. Although locations with warmer water temperatures were more prone to hybridization, cold sites were not protected from invasion; 58% of hybridized sites had cold mean summer water temperatures (<11°C). Despite cessation of stocking over 40 years ago, hybridization increased over time at half (50%) of the locations with long‐term data, the vast majority of which (74%) were initially nonhybridized, emphasizing the chronic, negative impacts of human‐mediated hybridization. These results show that effects of climate change on biodiversity must be analyzed in the context of historical human impacts that set ecological and evolutionary trajectories.

    

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2. Biased gene retention in the face of introgression obscures species relationships

   https://doi.org/10.1093/gbe/evaa149  

   Forsythe, Evan S ; Nelson, Andrew D ; Beilstein, Mark A ( July 2020 , Genome Biology and Evolution)

   Abstract Phylogenomic analyses are recovering previously hidden histories of hybridization, revealing the genomic consequences of these events on the architecture of extant genomes. We applied phylogenomic techniques and several complementary statistical tests to show that introgressive hybridization appears to have occurred between close relatives of Arabidopsis, resulting in cytonuclear discordance and impacting our understanding of species relationships in the group. The composition of introgressed and retained genes indicates that selection against incompatible cytonuclear and nuclear-nuclear interactions likely acted during introgression, while linkage also contributed to genome composition through the retention of ancient haplotype blocks. We also applied divergence-based tests to determine the species branching order and distinguish donor from recipient lineages. Surprisingly, these analyses suggest that cytonuclear discordance arose via extensive nuclear, rather than cytoplasmic, introgression. If true, this would mean that most of the nuclear genome was displaced during introgression, while only a small proportion of native alleles were retained. 

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3. Variable hybridization outcomes in trout are predicted by historical fish stocking and environmental context

   https://doi.org/10.1111/mec.15175  

   Mandeville, Elizabeth G. ; Walters, Annika W. ; Nordberg, Brittany J. ; Higgins, Karly H. ; Burckhardt, Jason C. ; Wagner, Catherine E. ( August 2019 , Molecular Ecology)

   Hybridization can profoundly affect the genomic composition and phenotypes of closely related species, and provides an opportunity to identify mechanisms that maintain reproductive isolation between species. Recent evidence suggests that hybridization outcomes within a species pair can vary across locations. However, we still do not know how variable outcomes of hybridization are across geographic replicates, and what mechanisms drive that variation. In this study, we described hybridization outcomes across 27 locations in the North Fork Shoshone River basin (Wyoming, USA) where native Yellowstone cutthroat trout and introduced rainbow trout co‐occur. We used genomic data and hierarchical Bayesian models to precisely identify ancestry of hybrid individuals. Hybridization outcomes varied across locations. In some locations, only rainbow trout and advanced backcrossed hybrids towards rainbow trout were present, while trout in other locations had a broader range of ancestry, including both parental species and first‐generation hybrids. Later‐generation intermediate hybrids were rare relative to backcrossed hybrids and rainbow trout individuals. Using an individual‐based simulation, we found that outcomes of hybridization in the North Fork Shoshone River basin deviate substantially from what we would expect under null expectations of random mating and no selection against hybrids. Since this deviation implies that some mechanisms of reproductive isolation function to maintain parental taxa and a diversity of hybrid types, we then modelled hybridization outcomes as a function of environmental variables and stocking history that are likely to affect prezygotic barriers to hybridization. Variables associated with history of fish stocking were the strongest predictors of hybridization outcomes, followed by environmental variables that might affect overlap in spawning time and location.

    

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4. Signals of differential introgression in the genome of natural hybrids of Caribbean anoles

   https://doi.org/10.1111/mec.17170  

   Farleigh, Keaka ; Ascanio, Alfredo ; Farleigh, Mackenzie E. ; Schield, Drew R. ; Card, Daren C. ; Leal, Manuel ; Castoe, Todd A. ; Jezkova, Tereza ; Rodríguez‐Robles, Javier A. ( October 2023 , Molecular Ecology)

   Hybridization facilitates recombination between divergent genetic lineages and can be shaped by both neutral and selective processes. Upon hybridization, loci with no net fitness effects introgress randomly from parental species into the genomes of hybrid individuals. Conversely, alleles from one parental species at some loci may provide a selective advantage to hybrids, resulting in patterns of introgression that do not conform to random expectations. We investigated genomic patterns of differential introgression in natural hybrids of two species of Caribbean anoles,Anolis pulchellusandA. krugiin Puerto Rico. Hybrids exhibitA. pulchellusphenotypes but possessA. krugimitochondrial DNA, originated from multiple, independent hybridization events, and appear to have replaced pureA. pulchellusacross a large area in western Puerto Rico. Combining genome‐wide SNP datasets with bioinformatic methods to identify signals of differential introgression in hybrids, we demonstrate that the genomes of hybrids are dominated bypulchellus‐derived alleles and show only 10%–20%A. krugiancestry. The majority ofA. krugiloci in hybrids exhibit a signal of non‐random differential introgression and include loci linked to genes involved in development and immune function. Three of these genes (delta like canonical notch ligand 1, jagged1 and notch receptor 1) affect cell differentiation and growth and interact with mitochondrial function. Our results suggest that differential non‐random introgression for a subset of loci may be driven by selection favouring the inheritance of compatible mitochondrial and nuclear‐encoded genes in hybrids.

    

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5. Assessing thermal adaptation using family‐based association and F ST outlier tests in a threatened trout species

   https://doi.org/10.1111/mec.15100  

   Amish, Stephen J. ; Ali, Omar ; Peacock, Mary ; Miller, Michael ; Robinson, Morgan ; Smith, Seth ; Luikart, Gordon ; Neville, Helen ( May 2019 , Molecular Ecology)

   Discovering genetic markers associated with phenotypic or ecological characteristics can improve our understanding of adaptation and guide conservation of key evolutionary traits. The Lahontan cutthroat trout (Oncorhynchus clarkii henshawi) of the northern Great Basin Desert, USA, demonstrated exceptional tolerance to high temperatures in the desert lakes where it resided historically. This trait is central to a conservation hatchery effort to protect the genetic legacy of the nearly extinct lake ecotype. We genotyped full‐sibling families from this conservation broodstock and samples from the only two remaining, thermally distinct, native lake populations at 4,644 new single nucleotide polymorphisms (SNPs). Family‐based genome‐wide association testing of the broodstock identified nine and 26 SNPs associated with thermal tolerance (p < 0.05 andp < 0.1), measured in a previous thermal challenge experiment. Genes near the associated SNPs had complex functions related to immunity, growth, metabolism and ion homeostasis. Principal component analysis using the thermotolerance‐related SNPs showed unexpected divergence between the conservation broodstock and the native lake populations at these loci.F_SToutlier tests on the native lake populations identified 18 loci shared between two or more of the tests, with two SNPs identified by all three tests (p < 0.01); none overlapped with loci identified by association testing in the broodstock. A recent history of isolation and the complex genetic and demographic backgrounds of Lahontan cutthroat trout probably limited our ability to find shared thermal tolerance loci. Our study extends the still relatively rare application of genomic tools testing for markers associated with important phenotypic or environmental characteristics in species of conservation concern.

    

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