Collaborative research: The genomic underpinnings of local adaptation despite gene flow along a coastal environmental cline

海洋是大而开放的栖息地，以前人们认为，海洋缺乏明显的扩散障碍，会导致广泛的混合，阻止生物在遗传上适应特定的栖息地。然而，最近已经清楚的是，许多海洋物种被细分为多个种群，这些种群在相互对比的当地环境条件下进化得最好。尽管如此，我们仍然对基因组机制知之甚少，这些机制在持续的混合中使不同的适应成为可能。该项目的重点是大西洋银汉鱼（Menidia menidia），这是一种小型河口鱼，在生长速度和一系列与跨纬度气候梯度密切相关的其他特征方面表现出显着的地方适应性。几十年的实验室和实地研究已经使大西洋银汉鱼成为海洋物种之一，我们对导致适应性分歧的性状和选择驱动因素之间的进化权衡有了最好的了解。然而，到目前为止，根本的基因组基础是完全未知的。研究人员将整合从分布范围内取样的野生鱼类的全基因组测序数据，并在实验室进行育种实验，以破译这些基因组基础。这将提供迄今为止对海洋局部适应的基因组基础的最全面评估之一，从而产生迫切需要的见解，以便更好地预测物种如何应对快速的环境变化。该项目将为一名博士后以及两名研究生和几名来自代表性不足的少数民族的本科生提供跨学科培训。研究结果亦会用作发展具吸引力的教学及外展材料（例如纪录短片及科普文章），以促进理科学生及公众对生态、进化及地方适应的认识。该项目的目标是描述M. menidia和研究适应性分歧是如何形成的不同水平的基因流，并保持在生态时间尺度。该项目分为四个相互关联的部分。第1部分考察了基因组分化的精细尺度空间模式，沿着适应性渐变群，以a）表征连接性景观，B）识别趋异选择下的基因组区域，以及c）通过考察等位基因频率如何与环境因素和地理特征相关而变化来推断选择的潜在驱动因素和目标。第2部分将关键的地方适应性状映射到基因组，以剖析其潜在的基因组基础。第3部分整合了野生环境中的变异模式（第1部分）和受控条件下的性状图谱（第2部分），以a）研究局部适应的基因组结构如何在基因流动机制中变化，以及B）阐明染色体重排和适应性等位基因之间的其他紧密连锁在促进适应中的潜在作用。最后，第4部分考察了季节性时间尺度上的扩散-选择动力学，以a）推断对迁移者及其后代的选择如何维持当地的适应，尽管有着明显的连通性，以及B）验证当地适应的候选位点。在物种范围内，不同水平的基因流创造了一个自然的实验，用于测试基因组机制的一般预测，这些机制使适应性分化在基因流面前成为可能。因此，这一发现将具有广泛的影响，并将大大促进我们对基因组结构在沿海环境中改变基因流-选择平衡中所起作用的理解。该奖项反映了NSF的法定使命，并被认为值得通过使用基金会的智力价值和更广泛的影响审查标准进行评估来支持。

Oceans are large, open habitats, and it was previously believed that their lack of obvious barriers to dispersal would result in extensive mixing, preventing organisms from adapting genetically to particular habitats. It has recently become clear, however, that many marine species are subdivided into multiple populations that have evolved to thrive best under contrasting local environmental conditions. Nevertheless, we still know very little about the genomic mechanisms that enable divergent adaptations in the face of ongoing intermixing. This project focuses on the Atlantic silverside (Menidia menidia), a small estuarine fish that exhibits a remarkable degree of local adaptation in growth rates and a suite of other traits tightly associated with a climatic gradient across latitudes. Decades of prior lab and field studies have made Atlantic silverside one of the marine species for which we have the best understanding of evolutionary tradeoffs among traits and drivers of selection causing adaptive divergence. Yet, the underlying genomic basis is so far completely unknown. The investigators will integrate whole genome sequencing data from wild fish sampled across the distribution range with breeding experiments in the laboratory to decipher these genomic underpinnings. This will provide one of the most comprehensive assessments of the genomic basis for local adaptation in the oceans to date, thereby generating insights that are urgently needed for better predictions about how species can respond to rapid environmental change. The project will provide interdisciplinary training for a postdoc as well as two graduate and several undergraduate students from underrepresented minorities. The findings will also be leveraged to develop engaging teaching and outreach materials (e.g. a video documentary and popular science articles) to promote a better understanding of ecology, evolution, and local adaptation among science students and the general public. The goal of the project is to characterize the genomic basis and architecture underlying local adaptation in M. menidia and examine how the adaptive divergence is shaped by varying levels of gene flow and maintained over ecological time scales. The project is organized into four interconnected components. Part 1 examines fine-scale spatial patterns of genomic differentiation along the adaptive cline to a) characterize the connectivity landscape, b) identify genomic regions under divergent selection, and c) deduce potential drivers and targets of selection by examining how allele frequencies vary in relation to environmental factors and biogeographic features. Part 2 maps key locally adapted traits to the genome to dissect their underlying genomic basis. Part 3 integrates patterns of variation in the wild (part 1) and the mapping of traits under controlled conditions (part 2) to a) examine how genomic architectures underlying local adaptation vary across gene flow regimes and b) elucidating the potential role of chromosomal rearrangements and other tight linkage among adaptive alleles in facilitating adaptation. Finally, part 4 examines dispersal - selection dynamics over seasonal time scales to a) infer how selection against migrants and their offspring maintains local adaptation despite homogenizing connectivity and b) validate candidate loci for local adaptation. Varying levels of gene flow across the species range create a natural experiment for testing general predictions about the genomic mechanisms that enable adaptive divergence in the face of gene flow. The findings will therefore have broad implications and will significantly advance our understanding of the role genomic architecture plays in modifying the gene flow - selection balance within coastal environments.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.