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Colella, J. P.

Publications and source records attributed to Colella, J. P..

9 recordsLinked to original sources

Mitochondrial introgression in North American red-backed voles is facilitated by co-introgression at nuclear-encoded mitochondrial genes

Mitochondrial genomes encode for the proteins and RNAs that serve as the basis for aerobic respiration and energy production. Yet mitochondria depend on the nuclear genome for hundreds of additional genes whose products engage in core metabolic processes (N-mt genes). Despite strong selective pressure for coevolved mitonuclear interactions, there are numerous examples of mitochondrial introgression across species barriers. Mitonuclear co-introgression, a process whereby alleles at N-mt genes move across species boundaries in concert with mitochondrial genomes, has been suggested as a mechanism whereby species could capture heterospecific mitochondria while avoiding mitonuclear incompatibilities, but evidence for this phenomenon is sparse. We test for evidence of mitonuclear co-introgression in two discordant populations of North American red-backed voles (Clethrionomys gapperi nuclear genomes, C. rutilus mitochondrial genomes) using whole genome resequencing. We find that N-mt genes in both populations are significantly enriched for C. rutilus ancestry, with evidence of co-introgression at eighteen N-mt genes. Notably, two N-mt genes directly associated with mitochondrial translation are fixed or nearly fixed for C. rutilus ancestry in both discordant populations and analyses of genetic variation at these genes suggest recent selective sweeps. We pair these findings with mitochondrial phylogenies, recent demographic histories, and recombination maps, which support a scenario of ongoing introgression in British Columbia but cessation of gene flow in Southeast Alaska. Together, our results show that mitochondrial introgression in North American red-backed voles is adaptive and that mitonuclear incompatibilities are avoided through mitonuclear co-introgression.

evolutionary biology↗

Selecting sites for strategic surveillance of zoonotic pathogens: a case study in Panama

Surveillance and monitoring of zoonotic pathogens is key to identifying and mitigating emerging public health threats. Surveillance is often designed to be taxonomically targeted or systematically dispersed across geography, however, those approaches may not represent the breadth of environments inhabited by a host, vector, or pathogen, leaving significant gaps in our understanding of pathogen dynamics in their natural reservoirs and environments. As a case study on the design of pathogen surveillance programs, we assess how well 20 years of small mammal surveys in Panama have sampled available environments and propose a multistep approach to selecting survey localities in the future. We use >8,000 georeferenced mammal specimen records, collected as part of a long-term hantavirus surveillance program, to test the completeness of country-wide environmental sampling. Despite 20 years of surveillance, our analyses identified a few key environmental sampling gaps. To refine surveillance strategies, we selected a series of core historically sampled localities, supplemented with additional environmentally distinct sites to more completely represent Panamas environments. Based on lessons learned through decades of surveillance, we propose a series of recommendations to improve strategic sampling for zoonotic pathogen surveillance.

ecology↗

That's not a Hybrid: How to Distinguish Patterns of Admixture and Isolation-by-Distance

Describing naturally occurring genetic variation is a fundamental goal of molecular phylogeography and population genetics. Popular methods for this task include STRUCTURE, a model-based algorithm that assigns individuals to genetic clusters, and Principal Component Analysis (PCA), a parameter-free method. The ability of STRUCTURE to infer mixed ancestry makes it popular for documenting natural hybridization, which is of considerable interest to evolutionary biologists, given that such systems provide a window into the speciation process. Yet STRUCTURE can produce misleading results when its underlying assumptions are violated, like when genetic variation is distributed continuously. To test the ability of STRUCTURE and PCA to accurately distinguish admixture from continuous variation, we use forward-time simulations to generate population genetic data under three demographic scenarios: two involving admixture and one with isolation-by-distance (IBD). STRUCTURE and PCA alone cannot distinguish admixture from IBD, but complementing these analyses with triangle plots, which visualize hybrid index against interclass heterozygosity, provides more accurate inference of demographic history. We demonstrate that triangle plots are robust to missing data, while STRUCTURE and PCA are not, and show that setting a low allele frequency difference threshold for AIM identification can accurately characterize the relationship between hybrid index and interclass heterozygosity across demographic histories of admixture and range expansion. While STRUCTURE and PCA provide useful summaries of genetic variation, results should be paired with triangle plots before admixture is inferred.

evolutionary biology↗

triangulaR: an R package for identifying AIMs and building triangle plots using SNP data from hybrid zones

Hybridization provides a window into the speciation process and reshuffles parental alleles to produce novel recombinant genotypes. The presence or absence of specific hybrid classes across a hybrid zone can provide support for various modes of reproductive isolation. Early generation hybrid classes can be distinguished by their combination of hybrid index and interclass heterozygosity, which can be estimated with molecular data. Hybrid index and interclass heterozygosity are routinely calculated for studies of hybrid zones, but available resources for next-generation sequencing datasets are computationally demanding and tools for visualizing those metrics as a triangle plot are lacking. Here, we provide a resource for identifying ancestry- informative markers (AIMs) from SNP datasets, calculating hybrid index and interclass heterozygosity, and visualizing the relationship as a triangle plot. Our methods are implemented in the R package triangulaR. We validate our methods by simulating genetic data for a hybrid zone between parental groups at low, medium, and high levels of divergence. We find that accurate and precise estimates of hybrid index and interclass heterozygosity can be obtained with sample sizes as low as five individuals per parental group. We explore various allele frequency difference thresholds for AIM identification, and how this threshold influences the accuracy and precision of hybrid index and interclass heterozygosity estimates. We contextualize interpretation of triangle plots by describing the theoretical expectations for covariance of hybrid index and interclass heterozygosity under Hardy-Weinberg Equilibrium and provide recommendations for best practices for identifying AIMs and building triangle plots.

evolutionary biology↗

High total water loss driven by low-fat diet in desert-adapted mice

Availability of food resources is an important driver of survival. Animals must either relocate or adapt to persist in environments where critical resource abundance is changing. An optimal diet balances energy gain, water regulation, and nutrition. We used flow-through respirometry to characterize metabolic phenotypes of the desert-adapted cactus mouse (Peromyscus eremicus) under diurnally variable environmental conditions that mimic the environment of the Sonoran Desert. We treated mice with two different energetically equivalent diets, a standard diet and a low-fat diet, and measured energy expenditure, water loss rate, respiratory quotient, weight, and electrolyte levels. Mice fed the low-fat diet lost significantly more water than those on the standard diet. Our results suggest that cactus mice may have limited capacity to tolerate water deprivation if optimal foods become less abundant. Given that climate change is predicted to modify the distribution of food items, understanding these links may have important implications for long-term population viability for desert and non-desert adapted animals alike.

physiology↗

Disentangling environmental drivers of circadian metabolism in desert-adapted mice

Metabolism is a complex phenotype shaped by natural environmental rhythms, as well as behavioral, morphological, and physiological adaptations. Although historically studied under constant environmental conditions, continuous metabolic phenotyping through environmental transitions now offers a window into the physiological responses of organisms to changing environments. Here, we use flow-through respirometry to compare metabolic responses of the desert-adapted cactus mouse (Peromyscus eremicus) between diurnally variable and constant environmental conditions. We contrast metabolic responses to circadian cycles in photoperiod, temperature, and humidity, against those recorded under constant hot-and-dry and constant cold-and-wet conditions. We found significant sexual dimorphism in metabolic responses, despite no measurable difference in body weight. Males seem to be more heat tolerant and females more cold tolerant. Under circadian environmental cycling, the ratio of CO2 produced to O2 consumed (the respiratory quotient or respiratory exchange ratio) reached greater than one, a pattern that strongly suggests that lipogenesis is contributing to the production of energy and endogenous water in this species. This hypothesis is consistent with the results of previous dehydration experiments in this species, which documented significant weight loss in response to dehydration, without other physiological impairment. Our results are also consistent with historical descriptions of circadian torpor in this species (torpid by day, active by night), but reject the hypothesis that this pattern is driven by food restriction or negative water balance, as both resources were available to animals throughout the experiments. SUMMARY STATEMENTContinuous metabolic phenotyping of desert-adapted cactus mice (Peromyscus eremicus) identifies significant metabolic differences between the sexes and circadian patterning consistent with lipogenesis and environmental entrainment.

physiology↗

Multiple evolutionary pathways to achieve thermal adaptation in small mammals

Phenotypic plasticity enables an immediate response to changing conditions, but for most species, evolutionary change through adaptation will be more important for long-term survival. Warming climate and increasing desertification urges the identification of genes involved in heat-and dehydration-tolerance to better inform and target biodiversity conservation efforts. Comparisons among extant desert adapted species can highlight parallel or convergent patterns of genome evolution through the identification of shared signatures of selection. We generate chromosome-level genome assembly for the canyon mouse (Peromyscus crinitus) and test for signature of parallel evolution by comparing signatures of selective sweeps across population-level genomic resequencing data from another desert specialist deer mouse (P. eremicus) and a widely-distributed habitat generalist (P. maniculatus), that may locally adapted to arid conditions. We identify few shared candidate loci involved in desert adaptation and do not find support for a shared pattern of parallel evolution. Instead, we hypothesize divergent molecular mechanisms of desert adaptation among deer mice, potentially tied to species-specific historical demography, which may limit or enhance adaptation. We identify a number of candidate loci experiencing selective sweeps in the P. crinitus genome that are implicated in osmoregulation (Trypsin, Prostasin) and metabolic regulation (Kallikrein, eIF2-alpha kinase GCN2, APPL1/2), which may be important to accommodating hot and dry environmental conditions.

evolutionary biology↗

Comparative and population genomics approaches reveal the basis of adaptation to deserts in a small rodent

Organisms that live in deserts offer the opportunity to investigate how species adapt to environmental conditions that are lethal to most plants and animals. In the hot deserts of North America, high temperatures and lack of water are conspicuous challenges for organisms living there. The cactus mouse (Peromyscus eremicus) displays several adaptations to these conditions, including low metabolic rate, heat tolerance, and the ability to maintain homeostasis under extreme dehydration. To investigate the genomic basis of desert adaptation in cactus mice, we built a chromosome-level genome assembly and resequenced 26 additional cactus mouse genomes from two locations in southern California (USA). Using these data, we integrated comparative, population, and functional genomic approaches. We identified 16 gene families exhibiting significant contractions or expansions in the cactus mouse compared to 17 other Myodontine rodent genomes, and found 232 sites across the genome associated with selective sweeps. Functional annotations of candidate gene families and selective sweeps revealed a pervasive signature of selection at genes involved in the synthesis and degradation of proteins, consistent with the evolution of cellular mechanisms to cope with protein denaturation caused by thermal and hyperosmotic stress. Other strong candidate genes included receptors for bitter taste, suggesting a dietary shift towards chemically defended desert plants and insects, and a growth factor involved in lipid metabolism, potentially involved in prevention of dehydration. Understanding how species adapted to the recent emergence of deserts in North America will provide an important foundation for predicting future evolutionary responses to increasing temperatures, droughts and desertification in the cactus mouse and other species.

evolutionary biology↗

Higher quality de novo genome assemblies from degraded museum specimens: a linked-read approach to museomics

AO_SCPLOWBSTRACTC_SCPLOWHigh-throughput sequencing technologies are a proposed solution for accessing the molecular data in historic specimens. However, degraded DNA combined with the computational demands of short-read assemblies has posed significant laboratory and bioinformatics challenges. Linked-read or synthetic long-read sequencing technologies, such as 10X Genomics, may provide a cost-effective alternative solution to assemble higher quality de novo genomes from degraded specimens. Here, we compare assembly quality (e.g., genome contiguity and completeness, presence of orthogroups) between four published genomes assembled from a single shotgun library and four deer mouse (Peromyscus spp.) genomes assembled using 10X Genomics technology. At a similar price-point, these approaches produce vastly different assemblies, with linked-read assemblies having overall higher quality, measured by larger N50 values and greater gene content. Although not without caveats, our results suggest that linked-read sequencing technologies may represent a viable option to build de novo genomes from historic museum specimens, which may prove particularly valuable for extinct, rare, or difficult to collect taxa.

genomics↗