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1. Few Fixed Variants between Trophic Specialist Pupfish Species Reveal Candidate Cis -Regulatory Alleles Underlying Rapid Craniofacial Divergence

   https://doi.org/10.1093/molbev/msaa218  

   McGirr, Joseph A ; Martin, Christopher H ( September 2020 , Molecular Biology and Evolution)

   Wittkopp, Patricia (Ed.)

   Abstract Investigating closely related species that rapidly evolved divergent feeding morphology is a powerful approach to identify genetic variation underlying variation in complex traits. This can also lead to the discovery of novel candidate genes influencing natural and clinical variation in human craniofacial phenotypes. We combined whole-genome resequencing of 258 individuals with 50 transcriptomes to identify candidate cis-acting genetic variation underlying rapidly evolving craniofacial phenotypes within an adaptive radiation of Cyprinodon pupfishes. This radiation consists of a dietary generalist species and two derived trophic niche specialists—a molluscivore and a scale-eating species. Despite extensive morphological divergence, these species only diverged 10 kya and produce fertile hybrids in the laboratory. Out of 9.3 million genome-wide SNPs and 80,012 structural variants, we found very few alleles fixed between species—only 157 SNPs and 87 deletions. Comparing gene expression across 38 purebred F1 offspring sampled at three early developmental stages, we identified 17 fixed variants within 10 kb of 12 genes that were highly differentially expressed between species. By measuring allele-specific expression in F1 hybrids from multiple crosses, we found that the majority of expression divergence between species was explained by trans-regulatory mechanisms. We also found strong evidence for two cis-regulatory alleles affecting expression divergence of two genes with putative effects on skeletal development (dync2li1 and pycr3). These results suggest that SNPs and structural variants contribute to the evolution of novel traits and highlight the utility of the San Salvador Island pupfish system as an evolutionary model for craniofacial development. 

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2. Tethered homing gene drives: A new design for spatially restricted population replacement and suppression

   https://doi.org/10.1111/eva.12827  

   Dhole, Sumit ; Lloyd, Alun L. ; Gould, Fred ( June 2019 , Evolutionary Applications)

   Optimism regarding potential epidemiological and conservation applications of modern gene drives is tempered by concern about the possibility of unintended spread of engineered organisms beyond the target population. In response, several novel gene drive approaches have been proposed that can, under certain conditions, locally alter characteristics of a population. One challenge for these gene drives is the difficulty of achieving high levels of localized population suppression without very large releases in the face of gene flow. We present a new gene drive system, tethered homing (TH), with improved capacity for both localization and population suppression. The TH drive is based on driving a payload gene using a homing construct that is anchored to a spatially restricted gene drive. We use a proof‐of‐concept mathematical model to show the dynamics of a TH drive that uses engineered underdominance as an anchor. This system is composed of a split homing drive and a two‐locus engineered underdominance drive linked to one part of the split drive (the Cas endonuclease). We use simple population genetic simulations to show that the tethered homing technique can offer improved localized spread of costly transgenic payload genes. Additionally, the TH system offers the ability to gradually adjust the genetic load in a population after the initial alteration, with minimal additional release effort. We discuss potential solutions for improving localization and the feasibility of creating TH drive systems. Further research with models that include additional biological details will be needed to better understand how TH drives would behave in natural populations, but the preliminary results shown here suggest that tethered homing drives can be a useful addition to the repertoire of localized gene drives.

    

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3. Nuclear eDNA estimates population allele frequencies and abundance in experimental mesocosms and field samples

   https://doi.org/10.1111/mec.15765  

   Andres, Kara J. ; Sethi, Suresh A. ; Lodge, David M. ; Andrés, Jose ( January 2021 , Molecular Ecology)

   Advances in environmental DNA (eDNA) methodologies have led to improvements in the ability to detect species and communities in aquatic environments, yet the majority of studies emphasize biological diversity at the species level by targeting variable sites within the mitochondrial genome. Here, we demonstrate that eDNA approaches also have the capacity to detect intraspecific diversity in the nuclear genome, allowing for assessments of population‐level allele frequencies and estimates of the number of genetic contributors in an eDNA sample. Using a panel of microsatellite loci developed for the round goby (Neogobius melanostomus), we tested the similarity between eDNA‐based and individual tissue‐based estimates of allele frequencies from experimental mesocosms and in a field‐based trial. Subsequently, we used a likelihood‐based DNA mixture framework to estimate the number of unique genetic contributors in eDNA samples and in simulated mixtures of alleles. In both mesocosm and field samples, allele frequencies from eDNA were highly correlated with allele frequencies from genotyped round goby tissue samples, indicating nuclear markers can be reliably amplified from water samples. DNA mixture analyses were able to estimate the number of genetic contributors from mesocosm eDNA samples and simulated mixtures of DNA from up to 58 individuals, with the degree of positive or negative bias dependent on the filtering scheme of low‐frequency alleles. With this study we document the application of eDNA and multiple amplicon‐based methods to obtain intraspecific nuclear genetic information and estimate the absolute abundance of a species in eDNA samples. With proper validation, this approach has the potential to advance noninvasive survey methods to characterize populations and detect population‐level genetic diversity.

    

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4. Multi‐population puma connectivity could restore genomic diversity to at‐risk coastal populations in California

   https://doi.org/10.1111/eva.13341  

   Gustafson, Kyle D. ; Gagne, Roderick B. ; Buchalski, Michael R. ; Vickers, T. Winston ; Riley, Seth P. D. ; Sikich, Jeff A. ; Rudd, Jaime L. ; Dellinger, Justin A. ; LaCava, Melanie E. F. ; Ernest, Holly B. ( January 2022 , Evolutionary Applications)

   Urbanization is decreasing wildlife habitat and connectivity worldwide, including for apex predators, such as the puma (Puma concolor). Puma populations along California's central and southern coastal habitats have experienced rapid fragmentation from development, leading to calls for demographic and genetic management. To address urgent conservation genomic concerns, we used double‐digest restriction‐site associated DNA (ddRAD) sequencing to analyze 16,285 genome‐wide single‐nucleotide polymorphisms (SNPs) from 401 pumas sampled broadly across the state. Our analyses indicated support for 4–10 geographically nested, broad‐ to fine‐scale genetic clusters. At the broadest scale, the four genetic clusters had high genetic diversity and exhibited low linkage disequilibrium, indicating that pumas have retained genomic diversity statewide. However, multiple lines of evidence indicated substructure, including 10 finer‐scale genetic clusters, some of which exhibited fixed alleles and linkage disequilibrium. Fragmented populations along the Southern Coast and Central Coast had particularly low genetic diversity and strong linkage disequilibrium, indicating genetic drift and close inbreeding. Our results demonstrate that genetically at risk populations are typically nested within a broader‐scale group of interconnected populations that collectively retain high genetic diversity and heterogenous fixations. Thus, extant variation at the broader scale has potential to restore diversity to local populations if management actions can enhance vital gene flow and recombine locally sequestered genetic diversity. These state‐ and genome‐wide results are critically important for science‐based conservation and management practices. Our nested population genomic analysis highlights the information that can be gained from population genomic studies aiming to provide guidance for the conservation of fragmented populations.

    

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5. Footprints of local adaptation span hundreds of linked genes in the Atlantic silverside genome

   https://doi.org/10.1002/evl3.189  

   Wilder, Aryn P. ; Palumbi, Stephen R. ; Conover, David O. ; Therkildsen, Nina Overgaard ( October 2020 , Evolution Letters)

   The study of local adaptation in the presence of ongoing gene flow is the study of natural selection in action, revealing the functional genetic diversity most relevant to contemporary pressures. In addition to individual genes, genome-wide architecture can itself evolve to enable adaptation. Distributed across a steep thermal gradient along the east coast of North America, Atlantic silversides (Menidia menidia) exhibit an extraordinary degree of local adaptation in a suite of traits, and the capacity for rapid adaptation from standing genetic variation, but we know little about the patterns of genomic variation across the species range that enable this remarkable adaptability. Here, we use low-coverage, whole-transcriptome sequencing of Atlantic silversides sampled along an environmental cline to show marked signatures of divergent selection across a gradient of neutral differentiation. Atlantic silversides sampled across 1371 km of the southern section of its distribution have very low genome-wide differentiation (median FST = 0.006 across 1.9 million variants), consistent with historical connectivity and observations of recent migrants. Yet almost 14,000 single nucleotide polymorphisms (SNPs) are nearly fixed (FST > 0.95) for alternate alleles. Highly differentiated SNPs cluster into four tight linkage disequilibrium (LD) blocks that span hundreds of genes and several megabases. Variants in these LD blocks are disproportionately nonsynonymous and concentrated in genes enriched for multiple functions related to known adaptations in silversides, including variation in lipid storage, metabolic rate, and spawning behavior. Elevated levels of absolute divergence and demographic modeling suggest selection maintaining divergence across these blocks under gene flow. These findings represent an extreme case of heterogeneity in levels of differentiation across the genome, and highlight how gene flow shapes genomic architecture in continuous populations. Locally adapted alleles may be common features of populations distributed along environmental gradients, and will likely be key to conserving variation to enable future responses to environmental change.

    

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