The first cavefish in the Dinaric Karst? Cave colonization made possible by phenotypic plasticity in Telestes karsticus

Zool Res. 2023 Jul 18;44(4):821-833. doi: 10.24272/j.issn.2095-8137.2022.528.

Abstract

Cave animals are an excellent model system for studying adaptive evolution. At present, however, little is known about the mechanisms that enable surface colonizers to survive in the challenging environment of caves. One possibility is that these species have the necessary genetic background to respond with plastic changes to the pressures of underground habitats. To gain insight into this process, we conducted a comparative study with the fish species Telestes karsticus, which occurs in a hydrological system consisting of an interconnected stream and a cave. Results showed that T. karsticus resided year-round and spawned in Sušik cave, making it the first known cavefish in the Dinaric Karst. Cave and surface populations differed in morphological and physiological characteristics, as well as in patterns of gene expression without any evidence of genetic divergence. To test whether observed trait differences were plastic or genetic, we placed adult fish from both populations under light/dark or constant dark conditions. Common laboratory conditions erased all morphometric differences between the two morphs, suggesting phenotypic plasticity is driving the divergence of shape and size in wild fish. Lighter pigmentation and increased fat deposition exhibited by cave individuals were also observed in surface fish kept in the dark in the laboratory. Our study also revealed that specialized cave traits were not solely attributed to developmental plasticity, but also arose from adult responses, including acclimatization. Thus, we conclude that T. karsticus can adapt to cave conditions, with phenotypic plasticity playing an important role in the process of cave colonization.

洞穴动物是研究适应性进化机制的绝佳模式系统。然而,目前人们对地表栖息物种在洞穴的挑战环境中生存的机制知之甚少。一种可能是,这些物种具有必要的遗传背景,能够以可塑性变化来应对地下栖息地的压力。为了深入了解这一过程,我们对生活在由相互连接的溪流和洞穴组成的水文系统中的鱼类 Telestes karsticus进行了比较研究。研究结果表明, Telestes karsticus常年栖息在Sušik洞穴中并在洞穴中产卵,这是在迪纳里喀斯特地区已知的第一种洞穴鱼。 洞穴种群和地表种群在形态和生理特征以及基因表达模式方面存在差异,但没有任何遗传分化的证据。为了检验观察到的性状差异是可塑性的还是遗传性的,我们将两个种群的成鱼置于光照/黑暗或持续黑暗的条件下。共同的实验室条件消除了两种形态之间的所有形态差异,表明表型可塑性是野生鱼类形状和大小分化的驱动力。在实验室黑暗条件下饲养的表层鱼类中也观察到洞穴个体表现出的浅色色素沉着和增加的脂肪沉积。我们的研究还发现,洞穴中的特化性状并不完全归因于发育的可塑性,也产生于成鱼的反应,包括适应。因此,克罗地亚侧带雅罗鱼具有适应洞穴环境的能力,其表型的可塑性在适应洞穴生存的过程中发挥了重要作用。.

Keywords: Acclimatization; Cave adaptations; Endemic leuciscid fish; European cavefish; Gene expression differences; Maladaptive and adaptive phenotypic plasticity; Troglobionts and stygobionts.

MeSH terms

  • Adaptation, Physiological
  • Animals
  • Biological Evolution
  • Caves*
  • Cypriniformes* / genetics
  • Phenotype
  • Pigmentation

Associated data

  • BioProject/PRJNA914542;GenBank:SAMN32340189-SAMN32340206

Grants and funding

This study was supported by the Tenure Track Pilot Programme of the Croatian Science Foundation and Ecole Polytechnique Fédérale de Lausanne and Project TTP-2018-07-9675 Evolution in the Dark, with funds from the Croatian-Swiss Research Programme (https://bilandzija.irb.hr/)