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

自然界最令人着迷的特征之一是当现有的结构具有新的功能或新的生态角色时，新颖性的进化。想想独角鲸的牙齿，天使鱼的诱饵，或者闪电甲虫发光的腹部。新奇是生命历史上重大转变的基础，包括从海洋到陆地的迁移，以及独特的哺乳动物特征的起源，如皮毛和哺乳。然而，这一过程的研究是具有挑战性的，因为新的转变通常不会在最早的阶段被观察到。错过早期阶段意味着错失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，它们非常适合进行此类研究。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、沉浸在研究中的课程。这些课程将为本科生提供有价值的统计编程和数据分析方面的培训。这项研究跨越了从基因到生态系统的范围，以解决一个基本问题：新颖性如何源于生态学、自然选择、性能和遗传学的交叉？回答这个问题是理解微观进化过程如何促进生命之树上新奇事物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，复杂的动力学导致了新颖性的进化。该项目将有助于弥合这两个领域之间的差距。为了做到这一点，这项研究将对新的向鳞片食肉和以蜗牛为食的转变进行实验研究。这两种摄食方式都起源于加勒比海鲤鱼的藻类祖先食谱。研究人员将采用：1)田间和实验室实验，测量不同环境中杂交表型的选择；2)生态系统规模的生产力测量；3)杂交性能的功能研究；4)适应性状遗传基础和适应变异来源的定量遗传和基因组分析。在实验室里将培育出不同品种的杂交鲤鱼。它们的适合性将在圣萨尔瓦多岛和邻近巴哈马群岛上高盐度湖泊的野外围栏内进行测量。将对这些湖泊的湖泊呼吸和大型藻类生物量进行测量，以评估资源丰度。与适应性营养形态相关的遗传变异的年龄和起源将使用全基因组重测序、遗传交叉、关联图谱和导入分析来调查。这一奖项反映了NSF的法定使命，并通过使用基金会的智力优势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.