CAREER: Cryptic origins of evolutionary novelty in Caribbean pupfishes: genomic, functional, and ecological conditions for crossing fitness valleys and colonizing adaptive peaks

自然界最迷人的特征之一是新奇的进化，当现有的结构承担新的功能或新的生态角色时。想想独角鲸的牙齿，琵琶鱼的诱饵，或者闪电甲虫发光的腹部。新颖性是生命史上重大转变的基础，包括从海洋到陆地的迁移，以及哺乳动物独特特征（如皮毛和哺乳）的起源。然而，这个过程的研究是具有挑战性的，因为新的转变通常不会在它们的最初阶段被观察到。错过早期阶段就意味着错过了进行实验研究的机会。这项研究将使用一组快速进化的鱼类来研究新的转变。由于这些鱼表现出新颖的骨骼结构，猎物捕获行为和生态位，它们非常适合此类研究。这个项目将产生基因如何控制面部结构和行为的基础知识；这些知识将有助于理解包括人类在内的所有脊椎动物的变异。此外，还将建立一个管理圈养濒危物种的公共数据库。将开发新的沉浸式研究课程。这些课程将为本科生提供统计编程和数据分析方面的宝贵训练。这项研究跨越了基因型和生态系统，以解决一个基本问题：新颖性是如何从生态学、自然选择、性能和遗传学的交叉中产生的？回答这个问题是理解微观进化过程如何促进整个生命之树中新颖的宏观进化模式的关键。传统的理解认为，新颖性源于新环境中的资源丰富。最近的实验室研究表明，复杂的动态导致了新颖性的进化。这个项目将有助于弥合这两个领域之间的差距。为此，该研究将通过实验研究食鳞和食蜗牛的新转变。这两种摄食方式都起源于加勒比海小鱼的藻类祖先饮食。研究人员将采用：1)实地和实验室实验，测量不同环境下杂交表型的选择；2)生态系统尺度的生产力测量；3)混合动力性能功能研究；4)适应性性状的遗传基础和适应性变异来源的定量遗传和基因组分析。幼鱼品种之间的杂交后代将在实验室中饲养。它们的健康状况将在圣萨尔瓦多岛和邻近的巴哈马群岛的高盐湖泊的野外围栏中进行测量。将测量湖泊呼吸和大型藻类生物量，以评估这些湖泊的资源丰度。与适应性营养形态相关的遗传变异的年龄和起源将通过全基因组重测序、遗传杂交、关联作图和渐渗分析进行研究。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。

One of the most fascinating features of the natural world is the evolution of novelty, when existing structures take on new functions or new ecological roles. Think of the narwhal's tooth, the anglerfish's lure, or the lightning beetle's glowing abdomen. Novelty underlies major transitions in the history of life, including moving from sea to land and the origins of unique mammalian traits such as fur and lactation. However, this process is challenging to study because novel transitions are not often observed at their earliest stages. Missing the early stages means missing out on the opportunity for experimental studies. This research will use a rapidly evolving group of fish to study novel transitions. Since these fish exhibit novel skeletal structures, prey capture behaviors, and ecological niches, they are well-suited for such studies. This project will produce fundamental knowledge of how genes control facial structures and behavior; this knowledge will be useful in understanding variation in all vertebrates, including humans. In addition, a public database for managing endangered species in captivity will be created. New, research-immersive courses will be developed. These courses will provide valuable training in statistical programming and data analysis for undergraduates.This research spans genotype to ecosystem to address a fundamental question: how does novelty originate from the intersection of ecology, natural selection, performance, and genetics? Answering this question is key to understanding how microevolutionary processes promote macroevolutionary patterns of novelty across the tree of life. Conventional understanding suggests novelty arises from resource abundance in new environments. More recent laboratory studies suggest complex dynamics lead to the evolution of novelty. This project will help bridge the gap between these two fields. To do so, the research will experimentally investigate novel transitions to scale-eating and snail-eating. Both feeding modes originated from an ancestral diet of algae in Caribbean pupfishes. The researchers will employ: 1) field and laboratory experiments measuring selection on hybrid phenotypes across environments; 2) ecosystem-scale measurements of productivity; 3) functional studies of hybrid performance; and 4) quantitative genetic and genomic analyses of the genetic basis of adaptive traits and source of adaptive variation. Hybrid crosses among pupfish species will be reared in the lab. Their fitness will be measured within field enclosures in hypersaline lakes on San Salvador Island and neighboring Bahamian islands. Lake respiration and macroalgae biomass will be measured across these lakes to assess resource abundance. The age and origin of genetic variation associated with adaptive trophic morphology will be investigated using whole-genome resequencing, genetic crosses, association mapping, and introgression analysis.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.