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，将导致广泛的混合，阻止生物从基因上适应特定的栖息地。然而，最近越来越清楚的是，许多海洋物种被细分为多个种群，这些种群在不同的当地环境条件下进化得最茁壮成长。尽管如此，我们仍然对基因组机制知之甚少，在面对持续的混合时，使不同的适应成为可能。这个项目的重点是大西洋银鱼（Menidia Menidia），这是一种小型的河口鱼类，在生长速度和一系列与纬度气候梯度密切相关的其他特征方面表现出显著的本地适应性。经过几十年的实验室和实地研究，大西洋银鱼是我们最了解特征和选择驱动因素之间的进化权衡的海洋物种之一，导致了适应性分化。然而，潜在的基因组基础到目前为止是完全未知的。研究人员将把从分布范围内取样的野生鱼类的全基因组测序数据与实验室的育种实验相结合，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最全面的评估之一，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、两名研究生和几名来自未被充分代表的少数民族的本科生提供跨学科培训。研究结果还将用于开发引人入胜的教学和推广材料（例如视频纪录片和科普文章），以促进理科生和公众更好地了解生态、进化和当地适应。该项目的目标是表征menidia局部适应的基因组基础和结构，并研究适应性差异是如何被不同水平的基因流塑造并在生态时间尺度上维持的。该项目被组织成四个相互关联的组件。第1部分研究了基因组分化的精细尺度空间格局，以a)表征连通性景观，b)识别不同选择下的基因组区域，以及c)通过研究等位基因频率与环境因素和生物地理特征的关系来推断潜在的选择驱动因素和目标。第2部分将关键的局部适应特征映射到基因组，以剖析其潜在的基因组基础。第3部分整合了野外变异模式（第1部分）和受控条件下的性状定位（第2部分），以a)研究不同基因流机制下本地适应的基因组结构如何变化；b)阐明染色体重排和适应等位基因之间的其他紧密联系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分散-选择动力学，以a)推断对迁移者及其后代的选择如何在同质化连通性的情况下保持本地适应性，b)验证候选基因座的本地适应性。跨越物种范围的不同水平的基因流动创造了一个自然的实验，用于测试关于基因组机制的一般预测，这些机制在面对基因流动时使适应性分化成为可能。因此，这些发现将具有广泛的意义，并将极大地促进我们对基因组结构在改变沿海环境中基因流动-选择平衡方面所起作用的理解。该奖项反映了美国国家科学基金会的法定使命，并通过使用基金会的知识价值和更广泛的影响审查标准进行评估，被认为值得支持。

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.