Genome-wide variation and transcriptional changes in diverse developmental processes underly the rapid evolution of seasonality

Short read data from study on variants associated with eclosion timing in Rhagoletis pomonella.Here, we present the results of an integrative study that leverages naturally segregating variation and a recent, adaptive divergence event affecting seasonal timing to identify developmental mechanisms underlying diapause progression in a tephritid fly, Rhagoletis pomonella. Also called the apple maggot fly, R. pomonella is native to North America, where it infests fruits of native Crataegus (hawthorn) species throughout its range. Derived populations of the fly infest apples (Malus domesticus), and thus have evolved in the last ~250 years since apples were introduced. Many molecular studies in conjunction with mark-recapture experiments document that the populations, or host races, remain genetically distinct despite ongoing gene flow, making R. pomonella a textbook example of incipient speciation with gene flow and host associated divergence. Strong natural selection on two primary traits, host finding behavior and seasonal timing, maintain genetic divergence. Both populations (hereafter apple and haw flies) have one generation per year, with a functionally obligate pupal diapause, overwintering in the soil. Adults must emerge coincident with host fruit availability, typically a period of only a few weeks, in order to successfully oviposit into fruits. Apple flies have evolved an earlier (~3 week) emergence timing to synchronize with apples, which fruit about 3 weeks earlier than hawthorn at a typical, sympatric site in the Midwest (e.g., Michigan or Illinois, USA). Previous analysis of genome-wide SNP variation suggested that emergence timing segregates as a polygenic trait, while comparison of host race transcriptomes at the end of winter suggested that host races diverge in diapause phenology during the winter, ultimately determining emergence timing during the late summer .We combined RNA sequencing (RNAseq), phenotyping of emergence timing and brain morphology, and whole genome pooled resequencing (Poolseq) to infer mechanisms underlying segregating variation for diapause phenology in each host race, and the evolved difference in phenology between host races.RNAseq data can be found on NCBI GEO GSE140473. This submission relates solely to short read data from poolseq.

本数据集源自针对苹果实蝇（Rhagoletis pomonella）羽化时间相关变异的研究。在此，我们呈现一项整合性研究的结果：该研究借助自然分离变异与近期发生的、影响季节节律的适应性分化事件，旨在阐明实蝇科昆虫苹果实蝇（Rhagoletis pomonella）滞育进程背后的发育机制。
该物种又名苹果蛆蝇，原产于北美，在其整个分布范围内均取食本土山楂属（Crataegus，亦称hawthorn）的果实。该蝇的衍生寄主种群则以苹果（Malus domesticus）为食，自苹果被引入北美至今的约250年间，该种群完成了适应性演化。多项结合标记-重捕实验的分子研究证实：尽管存在持续的基因交流，不同寄主种群（亦称寄主宗）仍维持遗传分化，这使得苹果实蝇成为兼具基因交流与寄主关联分化的初期物种形成的经典教科案例。针对寄主搜寻行为与季节节律这两个核心性状的强烈自然选择，维持了种群间的遗传分化。
两类寄主种群（下文分别简称苹果实蝇与山楂实蝇）均为一年一代，蛹期存在功能性专性滞育，并在土壤中越冬。成虫必须与寄主果实的可利用期同步羽化，而果实可利用期通常仅为数周，方能成功将卵产于果实内。苹果实蝇演化出了提前约3周的羽化节律，以匹配苹果的成熟期；在美国中西部（如密歇根州或伊利诺伊州）的典型同域分布位点中，苹果的结果时间比山楂早约3周。
此前针对全基因组单核苷酸多态性（Single Nucleotide Polymorphism, SNP）变异的分析表明，羽化时间属于多基因性状；而对冬末寄主宗转录组的比较研究则显示，寄主宗在冬季的滞育物候存在分化，这最终决定了夏末的羽化时间。本研究整合了RNA测序（RNAseq）、羽化时间与脑形态的表型分型，以及全基因组混合池重测序（Poolseq）技术，以推断各类寄主种群滞育物候的分离变异机制，以及不同寄主宗之间物候的演化差异。
RNA测序数据可在NCBI GEO数据库的GSE140473条目下获取。本提交仅包含混合池重测序的短读长数据。