Freda Philip J, Alex Jackson T, Morgan Theodore J, Ragland Gregory J
Department of Entomology, Kansas State University, Manhattan, KS 66502, USA.
Division of Biology, Kansas State University, Manhattan, KS 66502, USA.
Integr Comp Biol. 2017 Nov 1;57(5):999-1009. doi: 10.1093/icb/icx102.
As organisms age the environment fluctuates, exerting differential selection across ontogeny. In particular, highly seasonal environments expose life stages to often drastically different thermal environments. This developmental variation is particularly striking in organisms with complex life cycles, wherein life history stages also exhibit distinct morphologies, physiologies, and behaviors. Genes acting pleiotropically on thermal responses may produce genetic correlations across ontogeny, constraining the independent evolution of each life stage to their respective thermal environments. To investigate whether developmental genetic correlations constrain the evolution thermal hardiness of the fly Drosophila melanogaster, we applied quantitative genetic analyses to cold hardiness measured in both larvae and adults from isogenic lines of the Drosophila Genetic Reference Panel (DGRP), using survival at stressful low temperatures as the phenotypic metric. Using full genome resequencing data for the DGRP, we also implemented genome-wide association (GWA) analysis using Bayesian Sparse Linear Mixed Models (BSLMMs) to estimate associations between naturally segregating variation and cold hardiness for both larvae and adults. Quantitative genetic analyses revealed no significant genetic correlation for cold hardiness between life stages, suggesting complete genetic decoupling of thermal hardiness across the metamorphic boundary. Both quantitative genetic and GWA analyses suggested that polygenic variation underlies cold hardiness in both stages, and that associated loci largely affected one stage or the other, but not both. However, reciprocal enrichment tests and correlations between BSLMM parameters for each life stage support some shared physiological mechanisms that may reflect common cellular thermal response pathways. Overall, these results suggest no developmental genetic constraints on cold hardiness across metamorphosis in D. melanogaster, an important consideration in evolutionary models of responses to changing climates. Genetic correlations for environmental sensitivity across ontogeny remains largely unexplored in other organisms, thus assessing the generality of genetic decoupling will require further quantitative or population genetic analysis in additional species.
随着生物体衰老，环境会发生波动，在个体发育过程中施加差异选择。特别是，高度季节性的环境会使生命阶段暴露于往往截然不同的热环境中。这种发育变异在具有复杂生命周期的生物体中尤为显著，其中生命史阶段也表现出不同的形态、生理和行为。对热反应具有多效性作用的基因可能会在个体发育过程中产生遗传相关性，限制每个生命阶段独立进化以适应其各自的热环境。为了研究发育遗传相关性是否会限制果蝇黑腹果蝇耐寒性的进化，我们对果蝇遗传参考面板（DGRP）等基因系的幼虫和成虫的耐寒性进行了定量遗传分析，使用应激低温下的存活率作为表型指标。利用DGRP的全基因组重测序数据，我们还使用贝叶斯稀疏线性混合模型（BSLMM）进行全基因组关联（GWA）分析，以估计自然分离变异与幼虫和成虫耐寒性之间的关联。定量遗传分析表明，生命阶段之间的耐寒性没有显著的遗传相关性，这表明跨变态边界的热耐受性完全遗传解耦。定量遗传分析和GWA分析均表明，两个阶段的耐寒性都由多基因变异决定，且相关位点在很大程度上影响一个阶段或另一个阶段，但不是两者都影响。然而，每个生命阶段的BSLMM参数之间的相互富集测试和相关性支持一些共同的生理机制，这些机制可能反映了常见的细胞热反应途径。总体而言，这些结果表明，黑腹果蝇变态过程中的耐寒性不存在发育遗传限制，这是应对气候变化的进化模型中的一个重要考虑因素。其他生物体中个体发育过程中环境敏感性的遗传相关性在很大程度上仍未得到探索，因此评估遗传解耦的普遍性将需要在更多物种中进行进一步的定量或群体遗传分析。
