A priori and a posteriori approaches for finding genes of evolutionary interest in non-model species: Osmoregulatory genes in the kidney transcriptome of the desert rodent Dipodomys spectabilis (banner-tailed kangaroo rat)

Marra, Nicholas J.; Eo, Soo Hyung; Hale, Matthew C.; Waser, Peter M.; DeWoody, J. Andrew

doi:10.1016/j.cbd.2012.07.001

Cited by 38 publications

(52 citation statements)

References 72 publications

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“…The samples for this project were collected from the field as described in [43] and [35]. Briefly, spleen tissue from each of four adult D. spectabilis (2 males and 2 females) and four adult C. baileyi (2 males and 2 females) was harvested during collection trips to the same locale near Portal, AZ (about 31°37’N latitude) in December 2009 and December 2011, respectively.…”

Section: Methodsmentioning

confidence: 99%

“…For the D. spectabilis and H. desmarestianus samples, ½ plate of 454 sequencing was conducted using cDNA synthesized from our initial RNA extractions with the ClonTech SMART cDNA synthesis kit [44] with a modified CDS III/3’ primer (see [43, 45, 46]). For Illumina sequencing, fresh RNA extractions were used to obtain total RNA for all 12 samples, which were then purified using RNA Clean and Concentrator columns (Zymo Research).…”

Section: Methodsmentioning

confidence: 99%

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Transcriptomic characterization of the immunogenetic repertoires of heteromyid rodents

Marra

DeWoody

2014

BMC Genomics

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BackgroundWhen populations evolve under disparate environmental conditions, they experience different selective pressures that shape patterns of sequence evolution and gene expression. These may be manifested in genetic and phenotypic differences such as a diverse immunogenetic repertoire in species from tropical latitudes that have greater and/or different parasite burdens than more temperate species. To test this idea, we compared the transcriptomes of one tropical species (Heteromys desmarestianus) and two species from temperate latitudes (Dipodomys spectabilis and Chaetodipus baileyi) from the Heteromyidae. We did so in a search for positive selection on sequences and/or differential expression, while controlling for phylogenetic history in our choice of species.ResultsWe identified 127,812 contigs and annotated 34,878 of these, identifying immune genes associated with interleukins, cytokines, and the production of mast cells. We identified 632 genes that were upregulated in H. desmarestianus (8.7% of genes tested) and 492 (6.7%) that were downregulated. Gene ontology terms including “immune response” were associated with 31 (4.9%) of the 632 upregulated genes. We found preliminary evidence for positive selection on three genes (Palmitoyltransferase ZDHHC5 Ubiquitin-conjugating enzyme E2 N, Krueppel-like factor 10, and Spindle and kinetochore-associated protein 1) along the H. desmarestianus lineage.ConclusionsOverall our findings pinpoint genes in species from disparate environments that are on different evolutionary trajectories in terms of expression levels and/or nucleotide sequence. Our data indicate there are significant differences in the expression of genes among the spleen transcriptomes of these species and that a number of these differentially expressed genes do not show the same pattern of differential expression in another tissue type. This points to the possibility of expression differences between these species specific to the spleen transcriptome.Electronic supplementary materialThe online version of this article (doi:10.1186/1471-2164-15-929) contains supplementary material, which is available to authorized users.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Transcriptomic characterization of the immunogenetic repertoires of heteromyid rodents

Marra

DeWoody

2014

BMC Genomics

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“…High altitude adaptations to hemoglobin variants have been identified in multiple organisms, including humans (Lorenzo et al, 2014), several species of Andean ducks (McCracken et al, 2009a; McCracken et al, 2009b), and deer mice, Peromyscus maniculatus (Storz et al, 2010; Natarajan et al, 2015). The genetic pathways responsible for physiological adaptations to desert habitats remain enigmatic; however, considerable progress has been made developing candidate gene sets for future analyses (e.g., Guillen et al, 2015; MacManes & Eisen, 2014; Marra et al, 2012; Marra, Romero & DeWoody, 2014). Functional studies will stem from this foundational research aimed at identifying the genomic underpinnings of adaptations to extreme environments; yet, it is inherently challenging and critically important to demonstrate that specific loci are functionally responsible for adaptations (Storz & Wheat, 2010).…”

Section: Introductionmentioning

confidence: 99%

“…We propose that there may also be reproductive adaptations to mitigate water loss in desert rodents. Recent findings pertaining to the genetic signatures of adaptive kidney function in desert rodents (Marra et al, 2012; Marra, Romero & DeWoody, 2014; MacManes & Eisen, 2014), suggest that such hypothesized reproductive adaptations may be detectable at the genetic level (should they exist) using similar comparative transcriptomic methods. We present this hypothesis in light of the mounting body of research for high rates of reproductive protein evolution (reviewed in Swanson & Vacquier, 2002; Ramm et al, 2014), which we propose indicates that reproductive tissues may possess a significant capacity for evolving in response to strong selective pressures.…”

Section: Introductionmentioning

confidence: 99%

Characterization of a male reproductive transcriptome forPeromyscus eremicus(Cactus mouse)

Kordonowy

MacManes

2016

PeerJ

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Rodents of the genus Peromyscus have become increasingly utilized models for investigations into adaptive biology. This genus is particularly powerful for research linking genetics with adaptive physiology or behaviors, and recent research has capitalized on the unique opportunities afforded by the ecological diversity of these rodents. Well characterized genomic and transcriptomic data is intrinsic to explorations of the genetic architecture responsible for ecological adaptations. Therefore, this study characterizes the transcriptome of three male reproductive tissues (testes, epididymis and vas deferens) of Peromyscus eremicus (Cactus mouse), a desert specialist. The transcriptome assembly process was optimized in order to produce a high quality and substantially complete annotated transcriptome. This composite transcriptome was generated to characterize the expressed transcripts in the male reproductive tract of P. eremicus, which will serve as a crucial resource for future research investigating our hypothesis that the male Cactus mouse possesses an adaptive reproductive phenotype to mitigate water-loss from ejaculate. This study reports genes under positive selection in the male Cactus mouse reproductive transcriptome relative to transcriptomes from Peromyscus maniculatus (deer mouse) and Mus musculus. Thus, this study expands upon existing genetic research in this species, and we provide a high quality transcriptome to enable further explorations of our proposed hypothesis for male Cactus mouse reproductive adaptations to minimize seminal fluid loss.

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“…Although desert rodents must possess adaptations conferring survival and reproductive benefits, researchers have focused on their physiological adaptations for survival. For example, renal adaptations in species of Kangaroo rats (Dipodomys species) have been described and explored for over 60 years [27][28][29][30]. While early research determined the renal physiology for Kangaroo rats [27,29,31], recent research has focused on the genetic underpinnings of this phenotype [28,30,32], which is indicative of a larger methodological shift in the approach for examining adaptation.…”

Section: Introductionmentioning

confidence: 99%

Characterizing the reproductive transcriptomic correlates of acute dehydration in males in the desert-adapted rodent,Peromyscus eremicus

Kordonowy

MacManes

2016

Preprint

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Background: 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). Results: 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. Conclusions: 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.

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A priori and a posteriori approaches for finding genes of evolutionary interest in non-model species: Osmoregulatory genes in the kidney transcriptome of the desert rodent Dipodomys spectabilis (banner-tailed kangaroo rat)

Cited by 38 publications

References 72 publications

Transcriptomic characterization of the immunogenetic repertoires of heteromyid rodents

Transcriptomic characterization of the immunogenetic repertoires of heteromyid rodents

Characterization of a male reproductive transcriptome forPeromyscus eremicus(Cactus mouse)

Characterizing the reproductive transcriptomic correlates of acute dehydration in males in the desert-adapted rodent,Peromyscus eremicus

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