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

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.

背景：解析极端环境生物生存与繁殖相关的基因组及生理机制，是进化生物学与个体生物学研究者面临的核心科学议题。其中一个备受关注的适应性演化案例，与沙漠环境中的哺乳动物生存策略相关——沙漠环境普遍存在极端缺水的情况。现有针对沙漠啮齿动物适应性演化的研究，主要聚焦于其耐受脱水的适应性机制，而针对急性与慢性脱水的生殖生理适应性研究则相对匮乏。本研究以特化于沙漠环境的仙人掌鼠（Peromyscus eremicus）为研究对象，利用RNA测序（RNAseq）数据探究急性脱水对其生殖系统的影响。
结果：本研究将22只雄性仙人掌鼠随机分为两组，分别施加急性脱水处理与对照组（完全水合状态）处理；随后将睾丸来源的测序读段准映射至仙人掌鼠睾丸转录组，并分析差异转录本与基因表达模式。经多套分析流程进行统计学检验后，我们发现水合组与脱水组小鼠间共有9个基因呈现稳定的差异表达。我们此前曾提出假设：雄性仙人掌鼠对脱水的生殖响应极为有限；因此，两组间差异表达基因数量较少这一结果，与该物种高度特化的沙漠适应性认知相符。不过，本次鉴定到的差异表达基因包含胰岛素样蛋白3（Insulin-like 3, Insl3）——一种调控雄性生育能力与睾丸下降的关键因子，以及溶质载体家族蛋白Slc45a3与Slc38a5；二者均为膜转运蛋白，可能参与渗透压调节过程。
结论：本研究结果表明，在雄性仙人掌鼠中，急性脱水可能通过Insl3参与生殖调控，但并未影响其他预设检测的生殖激素相关基因的表达差异。尽管对于长期处于干旱环境的沙漠啮齿动物而言，水分可获得性是重要的生殖调控信号，但对于一种无需依赖外界水源即可全年存活并成功繁殖的物种来说，通过Insl3响应急性缺水以实现生殖调控的发现仍属意外。本研究亦凸显了开展整合性研究的必要性——需全面解析有机体适应性演化的各个维度；尤其在全球气候变化的背景下，气候变化不仅会加剧气候波动，还会使沙漠动物更频繁地遭遇本研究中所探讨的急性干旱胁迫。