Genome Evolution in Polar Fishes

Fish that reside in the harsh, subfreezing waters of the Antarctic and Arctic provide fascinating examples of adaptation to extreme environments. Species at both poles have independently evolved ways to deal with constant cold temperature, including the evolution of antifreeze proteins. Under freezing conditions, these compounds attach to ice crystals and prevent their growth. This lowers the tissue freezing point and reduces the chance the animal will be injured or killed. While it might seem that the need for unique adaptations to survive in polar waters would reduce species diversity in these habitats, recent evidence showed higher speciation rates in fishes from polar environments as compared to those found in warmer waters. This is despite the fact cold temperatures slow cellular processes, which had been expected to lower rates of molecular evolution in these species. To determine how rates of speciation and molecular evolution are linked in marine fishes, this project will compare the genomes of multiple polar and non-polar fishes. By doing so, it will (1) clarify how rates of evolution vary in polar environments, (2) identify general trends that shape the adaptive trajectories of polar fishes, and (3) determine how functional differences shape the evolution of novel compounds such as the antifreeze proteins some polar fishes rely upon to survive. In addition to training a new generation of scientists, the project will develop curriculum and outreach activities for elementary and undergraduate science courses. Materials will be delivered in classrooms across the western United States, with a focus on rural schools as part of a network for promoting evolutionary education in rural communities. To better understand the biology of polar fishes and the evolution of antifreeze proteins (AFPs), this research will compare the evolutionary histories of cold-adapted organisms to those of related non-polar species from both a genotypic and phenotypic context. In doing so, this research will test whether evolutionary rates are slowed in polar environments, perhaps due to constraints on cellular processes. It will also evaluate the effects of positive selection and the relaxation of selection on genes and pathways, both of which appear to be key adaptive strategies involved in the adaptation to polar environments. To address specific mechanisms by which extreme adaptation occurs, researchers will determine how global gradients of temperature and dissolved oxygen shape genome variation and influence adaptive trajectories among multiple species of eelpouts (family Zoarcidae). An in-vitro experimental approach will then be used to test functional hypotheses about the role of copy number variation in AFP evolution, and how and why multiple antifreeze protein isoforms have evolved. By comparing the genomes of multiple polar and non-polar fishes, the project will clarify how rates of evolution vary in polar environments, identify general trends that shape the adaptive trajectories of cold-adapted marine fishes, and determine how functional differences shape the evolution of novel proteins. This project addresses the strategic programmatic aim to provide a better understanding of the genetic underpinnings of organismal adaptations to their current environment and ways in which polar fishes may respond to changing conditions over different evolutionary time scales. The project is jointly funded by the Antarctic Organisms and Ecosystems Program in the Office of Polar Programs of the Geosciences Directorate, and the Molecular Biophysics Program of the Division of Molecular and Cellular Biosciences in the Biological Sciences Directorate. 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.

栖息于南极与北极严酷的亚冰冻水域的鱼类，是适应极端环境的极具启发性的研究范例。南北极海域的鱼类各自独立演化出应对持续低温的策略，其中便包括抗冻蛋白的演化。在冰冻环境下，这类化合物会附着于冰晶表面，抑制冰晶生长，从而降低组织冰点，减少鱼类因结冰而受伤或死亡的风险。

尽管人们或会认为，极地水域生存所需的独特适应性演化会压低此类生境的物种多样性，但近期研究证据表明，相较于温暖水域的鱼类，极地鱼类的物种形成速率反而更高。这一发现与此前的预期相悖：低温会减缓细胞代谢过程，本应降低这些物种的分子演化速率。为探明海洋鱼类的物种形成速率与分子演化速率之间的关联机制，本项目将对多种极地与非极地鱼类的基因组开展比较分析。通过此项研究，将实现三大目标：(1)阐明极地环境下演化速率的变化规律；(2)揭示塑造极地鱼类适应性演化轨迹的普遍趋势；(3)明确功能差异如何推动新型化合物的演化——例如部分极地鱼类赖以生存的抗冻蛋白。除培养新一代科研人才外，本项目还将为中小学及本科科学课程开发配套教学资源与科普活动。相关教学材料将在美国西部各地课堂推广使用，重点覆盖乡村学校，作为推动乡村社区进化生物学教育网络建设的组成部分。

为更深入地理解极地鱼类的生物学特性以及抗冻蛋白（antifreeze proteins, AFPs）的演化机制，本研究将从基因型与表型双重视角，对比分析冷适应生物与相关非极地产物种群的演化历史。借此，本研究将验证极地环境下演化速率是否因细胞过程受限而减缓，并评估正向选择与选择松弛对基因及通路的影响——二者均为极地适应的关键适应性策略。为阐明极端适应发生的具体机制，研究人员将探明温度与溶解氧的全球梯度如何影响绵鳚科（Zoarcidae）多个物种的基因组变异，并左右其适应性演化轨迹。后续将采用体外实验方法，验证关于拷贝数变异在抗冻蛋白演化中作用的功能假说，以及多种抗冻蛋白亚型的演化路径与动因。

通过对多种极地与非极地鱼类的基因组进行比较分析，本项目将阐明极地环境下演化速率的变化规律，揭示塑造冷适应海洋鱼类适应性演化轨迹的普遍趋势，并明确功能差异如何推动新型蛋白质的演化。本项目契合当前战略规划目标，即深化对生物体适应现有环境的遗传基础的理解，以及极地鱼类在不同演化时间尺度下响应环境变化的潜在路径。本项目由美国国家科学基金会（National Science Foundation, NSF）地球科学理事会极地项目办公室下辖的南极生物与生态系统项目，以及生物科学理事会分子与细胞生物科学分部的分子生物物理项目联合资助。

本奖项契合美国国家科学基金会的法定使命，并通过基金会的“智力价值”与“更广泛影响”两项评审标准的评估，认定其具备资助价值。