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MacManes, M.

Publications and source records attributed to MacManes, M..

9 recordsLinked to original sources

Evolution and Diversification of the Aposematic Poison Frog, Oophaga pumilio, in Bocas del Toro

The aposematic strawberry poison frog, Oophaga pumilio, is an iconic model system for studying the evolution and maintenance of color variation. Through most of its range, this frog is red with blue limbs. However, frogs from the Bocas del Toro Province, Panama, show striking variance in color and pattern, both sympatrically and allopatrically. This observation contradicts standard models of the evolution of aposematism and has led to substantial speculation about its evolutionary and molecular causes. Since the enigma of O. pumilio phenotypic variation is partly unresolved because of its large, [~] 6.7 Gb genome, we here sequence exomes from 347 individuals from ten populations and map a number of genetic factors responsible for the color and pattern variation. The kit gene is the primary candidate underlying the blue-red polymorphism in Dolphin Bay, where an increase in melanosomes is correlated with blue coloration. Additionally, the ttc39b gene, a known enhancer of yellow-to-red carotenoid conversion in birds, is the primary factor behind the yellow-red polymorphism in the Bastimentos West area. The causal genetic regions show evidence of selective sweeps acting locally to spread the rare phenotype. Our analyses suggest an evolutionary model in which selection is driving the formation of new morphs in a dynamic system resulting from a trade-off between predation avoidance, intraspecific competition, and mate choice.

evolutionary biology↗

When the tap runs dry: The multi-tissue gene expression and physiological responses of water deprived Peromyscus eremicus

The harsh and dry conditions of desert environments have resulted in genomic adaptations, allowing for desert organisms to withstand prolonged drought, extreme temperatures, and limited food resources. Here, we present a comprehensive exploration of gene expression across five tissues (kidney, liver, lung, gastrointestinal tract, and hypothalamus) and 19 phenotypic measurements to explore the whole-organism physiological and genomic response to water deprivation in the desert-adapted cactus mouse (Peromyscus eremicus). The findings encompass the identification of differentially expressed genes and correlative analysis between phenotypes and gene expression patterns across multiple tissues. Specifically, we found robust activation of the vasopressin renin-angiotensin-aldosterone system (RAAS) pathways, whose primary function is to manage water and solute balance. Animals reduce food intake during water deprivation, and upregulation of PCK1 highlights the adaptive response to reduced oral intake via its actions aimed at maintained serum glucose levels. Even with such responses to maintain water balance, hemoconcentration still occurred, prompting a protective downregulation of genes responsible for the production of clotting factors while simultaneously enhancing angiogenesis which is thought to maintains tissue perfusion. In this study, we elucidate the complex mechanisms involved in water balance in the desert-adapted cactus mouse, P. eremicus. By prioritizing a comprehensive analysis of whole-organism physiology and multi-tissue gene expression in a simulated desert environment, we describe the complex and successful response of regulatory processes.

genomics↗

Isolating the role of corticosterone in the hypothalamic-pituitary-gonadal genomic stress response

The negative impacts of stress on reproduction have long been studied. A large focus of investigation has centered around the effects of the adrenal steroid hormone corticosterone (CORT) on a system of tissues vital for reproduction, the hypothalamus of the brain, the pituitary gland, and the gonads (the HPG axis). Investigations of the role of CORT on the HPG axis have predominated the stress and reproductive biology literature, potentially overshadowing other influential mediators. To gain a more complete understanding of how elevated CORT, characteristic of the stress response, affects the activity of the HPG axis, we experimentally examined its role at the level of the genome in both male and female rock doves (Columba livia). We exogenously administrated CORT to mimic circulating levels during the stress response, specifically 30 min of restraint stress, an experimental paradigm known to increase circulating corticosterone in vertebrates. We examined all changes in genomic transcription within the HPG axis as compared to both restraint-stressed birds and vehicle-injected controls, as well as between the sexes. We report causal and sex-specific effects of CORT on the HPG stress response at the level of the transcriptome. Restraint stress caused 1567 genes to uniquely differentially express while elevated circulating CORT was responsible for the differential expression of 304 genes. Only 108 genes in females and 8 in males differentially expressed in subjects who underwent restraint stress and those who were given exogenous CORT. In response to CORT elevation characteristic of the stress response, both sexes shared the differential expression of 5 genes, KCNJ5, CISH, PTGER3, CEBPD, and ZBTB16, all located in the pituitary. The known functions of these genes suggest potential influence of elevated CORT on immune function and prolactin synthesis. Gene expression unique to each sex indicated that elevated CORT affected more gene transcription in females than males (78 genes versus 3 genes, respectively). To our knowledge, this is the first study to isolate the role of CORT in HPG genomic transcription during a stress response. These results provide novel targets for new lines of further investigation and therapy development. We present an extensive and openly accessible view of the role corticosterone in the HPG genomic stress response, offering novel gene targets to inspire new lines of investigation of stress-induced reproductive dysfunction. Because the HPG system is well-conserved across vertebrates, these data have the potential to inspire new therapeutic strategies for reproductive dysregulation in multiple vertebrate systems, including our own.

physiology↗

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↗

Divergent selection and drift shape the genomes of two avian sister species spanning a saline-freshwater ecotone

The role of species divergence due to ecologically-based divergent selection - or ecological speciation - in generating and maintaining biodiversity is a central question in evolutionary biology. Comparison of the genomes of phylogenetically related taxa spanning a selective habitat gradient enables discovery of divergent signatures of selection and thereby provides valuable insight into the role of divergent ecological selection in speciation. Tidal marsh ecosystems provide tractable opportunities for studying organisms adaptations to selective pressures that underlie ecological divergence. Sharp environmental gradients across the saline-freshwater ecotone within tidal marshes present extreme adaptive challenges to terrestrial vertebrates. Here we sequence 20 whole genomes of two avian sister species endemic to tidal marshes - the Saltmarsh Sparrow (Ammodramus caudacutus) and Nelsons Sparrow (A. nelsoni) - to evaluate the influence of selective and demographic processes in shaping genome-wide patterns of divergence. Genome-wide divergence between these two recently diverged sister species was notably high (genome-wide FST = 0.32). Against a background of high genome-wide divergence, regions of elevated divergence were widespread throughout the genome, as opposed to focused within islands of differentiation. These patterns may be the result of genetic drift acting during past tidal march colonization events in addition to divergent selection to different environments. We identified several candidate genes that exhibited elevated divergence between Saltmarsh and Nelsons sparrows, including genes linked to osmotic regulation, circadian rhythm, and plumage melanism - all putative candidates linked to adaptation to tidal marsh environments. These findings provide new insights into the roles of divergent selection and genetic drift in generating and maintaining biodiversity.

evolutionary biology↗

Transcriptomic analyses reveal tissue-specific selection on genes related to apoptotic processes in the subterranean rodent, Ctenomys sociabilis

Specialization for a subterranean existence is expected to impact multiple aspects of an organisms biology, including behavior, physiology, and genomic structure. While the phenotypic correlates of life underground have been extensively characterized, the genetic bases for these traits are not well understood, due in part to the challenges of generating large, multi-locus data sets using traditional DNA sequencing strategies. To begin exploring the genomic architecture of adaptation to a subterranean existence, we generated high-quality de novo transcriptome assemblies for 8 different tissue types (hippocampus, hypothalamus, kidney, liver, spleen, ovary, testis, skin) obtained from the colonial tuco-tuco (Ctenomys sociabilis), a group-living species of subterranean rodent that is endemic to southwestern Argentina. From these transcriptomes, we identified genes that are evolving more rapidly in the C. sociabilis lineage compared to other subterranean species of rodents. These comparisons suggest that genes associated with immune response, cell-cycle regulation, and heavy metal detoxification have been subject to positive selection in C. sociabilis. Comparisons of transcripts from different tissues suggest that the spleen and liver - organs involved in immune function and detoxification - may be particularly important sites for these adaptations, thereby underscoring the importance of including multiple tissue types in analyses of transcriptomic variation. In addition to providing an important resource for future genomic studies of C. sociabilis, our analyses generate new insights into the genomic architecture of functionally significant phenotypic traits in free-living mammals.

genomics↗

Transcriptomic Evidence for Reproductive Suppression in Male Peromyscus eremicus (Cactus Mouse) Subjected to Acute Dehydration

The understanding of genomic and physiological mechanisms related to how organisms living in extreme environments survive and reproduce is an outstanding question facing evolutionary and organismal biologists. One interesting example of adaptation is related to the survival of mammals in deserts, where extreme water limitation is common. Research on desert rodent adaptations has focused predominantly on adaptations related to surviving dehydration, while potential reproductive physiology adaptations for acute and chronic dehydration have been relatively neglected. This study aims to explore the reproductive consequences of acute dehydration by utilizing RNAseq data in the desert-specialized cactus mouse (Peromyscus eremicus). Specifically, we exposed 22 male cactus mice to either acute dehydration or control (fully hydrated) treatment conditions, quasimapped testes-derived reads to a cactus mouse testes transcriptome, and then evaluated patterns of differential transcript and gene expression. Following statistical evaluation with multiple analytical pipelines, nine genes were consistently differentially expressed between the hydrated and dehydrated mice. We hypothesized that male cactus mice would exhibit minimal reproductive responses to dehydration; therefore, this low number of differentially expressed genes between treatments aligns with current perceptions of this species extreme desert specialization. However, these differentially expressed genes include Insulin-like 3 (Insl3), a regulator of male fertility and testes descent, as well as the solute carriers Slc45a3 and Slc38a5, which are membrane transport proteins that may facilitate osmoregulation. Together, these results suggest that in male cactus mice, acute dehydration may be linked to reproductive modulation via Insl3, but not through gene expression differences in the subset of other a priori tested reproductive hormones. Although water availability is a reproductive cue in desert-rodents exposed to chronic drought, potential reproductive modification via Insl3 in response to acute water-limitation is a result which is unexpected in an animal capable of surviving and successfully reproducing year-round without available external water sources. Indeed, this work highlights the critical need for integrative research that examines every facet of organismal adaptation, particularly in light of global climate change, which is predicted, amongst other things, to increase climate variability, thereby exposing desert animals more frequently to the acute drought conditions explored here.

evolutionary biology↗

Comparative genomics of beetle-vectored fungal pathogens reveals a reduction in genome size and independent evolution of pathogenicity of two tree pathogens

O_LIGeosmithia morbida is an emerging fungal pathogen which serves as a paradigm for examining the evolutionary processes behind pathogenicity because it is one of two known pathogens within a genus of mostly saprophytic, beetle-associated, fungi. This pathogen causes thousand cankers disease in black walnut trees and is vectored into the host via the walnut twig beetle. G. morbida was first detected in western US and currently threatens the timber industry concentrated in eastern US.\nC_LIO_LIWe sequenced the genomes of G. morbida and two non-pathogenic Geosmithia species and compared these species to other fungal pathogens and nonpathogens to identify genes under positive selection in G. morbida that may be associated with pathogenicity.\nC_LIO_LIG. morbida possesses one of the smallest genomes among the fungal species observed in this study, and one of the smallest fungal pathogen genomes to date. The enzymatic profile is this pathogen is very similar to its relatives.\nC_LIO_LIOur findings indicate that genome reduction is an important adaptation during the evolution of a specialized lifestyle in fungal species that occupy a specific niche, such as beetle vectored tree pathogens. We also present potential genes under selection in G. morbida that could be important for adaptation to a pathogenic lifestyle.\nC_LI

evolutionary biology↗

Transcriptomics reveals patterns of sexually dimorphic gene expression in an avian hypothalamic-pituitary-gonadal (HPG) axis

The hypothalamic-pituitary-gonadal (HPG) axis is a key biological system required for reproduction and associated sexual behaviors to occur. Each of these tissues, the hypothalamus in the brain, the pituitary gland, and the gonads (testes and ovaries), has specialized and sometimes sex-specific functions that promote, amongst other things, reproductive processes. To fully characterize the transcript community of each aspect of the HPG axis, as well as to uncover potentially important sex-specific differences, we characterized patterns of gene expression in sexually mature male and female rock dove (Columba livia) hypothalamus, pituitary, and gonads. We describe patterns of gene expression amongst tissues as well as patterns of sex-biased gene expression which may underlie some of the fundamental differences between male and female reproductive behavior. We report greater sex-biased differential expression in the pituitary (233 genes out of 15,102 genes) as compared to the hypothalamus (1 gene out of 15,102 genes), with multiple genes overexpressed in the male pituitary gland being related to locomotion, and multiple genes over-expressed in the female pituitary gland being related to reproduction, growth and development. These genes may be associated with facilitating the different roles the HPG system plays in sex-specific reproductive behavior, including life-history strategies characterized by short-term payoffs in males (i.e. locomotion) and longer-term payoffs in females (i.e. development and reproduction). In addition, we report novel patterns of sex-biased expression in genes involved in reproduction-associated processes. Gonadotropin-releasing hormone, Progesterone, and Androgen receptor were upregulated in the female pituitary as compared to the male pituitary. We also found greater expression of Prolactin in the female pituitary as compared to the male pituitary, but it was more highly expressed in the male hypothalamus as compared to the female hypothalamus. The Prolactin receptor was also more highly expressed in the male hypothalamus and pituitary gland as compared to corresponding female tissues. Finally, we discovered greater expression of Arginine Vasopressin Receptor 1A in the male pituitary as compared to the female pituitary. Using a more global analysis, we discovered other interesting sex-biased patterns in genes not originally targeted for investigation. These genes include like Betacellulin (BTC), which was upregulated in the female pituitary and compared to males, and Ecto-NOX Disulfide-Thiol Exchanger 1 (ENOX1), which was upregulated in the male pituitary as compared to females. These genes may play important, though currently unknown, roles in reproductive physiology and behavior. In conclusion, we reveal patterns of tissue specific and sexually dimorphic gene expression in the HPG axis, highlighting the need for sex parity in transcriptomic studies and providing new lines of investigation of the mechanisms of reproductive function.

neuroscience↗