A widely accepted model for the evolution of cave animals posits colonization by surface ancestors followed by the acquisition of adaptations over many generations. However, the speed of cave adaptation in some species suggests mechanisms operating over shorter timescales. To address these mechanisms, we used Astyanax mexicanus, a teleost with ancestral surface morphs (surface fish, SF) and derived cave morphs (cavefish, CF). We exposed SF to completely dark conditions and identified numerous altered traits at both the gene expression and phenotypic levels. Remarkably, most of these alterations mimicked CF phenotypes. Our results indicate that many cave-related traits can appear within a single generation by phenotypic plasticity. In the next generation, plasticity can be further refined. The initial plastic responses are random in adaptive outcome but may determine the subsequent course of evolution. Our study suggests that phenotypic plasticity contributes to the rapid evolution of cave-related traits in A. mexicanus.
A widely accepted model for the evolution of cave animals posits colonization by surface ancestors followed by the acquisition of adaptations over many generations. However, the speed of cave adaptation in some species suggests mechanisms operating over shorter timescales. To address these mechanisms, we used Astyanax mexicanus, a teleost with ancestral surface morphs (surface fish, SF) and derived cave morphs (cavefish, CF). We exposed SF to completely dark conditions and identified numerous altered traits at both the gene expression and phenotypic levels. Remarkably, most of these alterations mimicked CF phenotypes. Our results indicate that cave-related traits can appear within a single generation by phenotypic plasticity. In the next generation, plasticity can be further refined. The initial plastic responses are random in adaptive outcome but may determine the subsequent course of evolution. Our study suggests that phenotypic plasticity contributes to the rapid evolution of cave-related traits in A. mexicanus. INTRODUCTION 1A major problem in modern biology is understanding how organisms adapt to an 2 environmental change and how complex, adaptive phenotypes originate. Phenotypic 3 evolution can result from standing genetic variation, new mutations, or phenotypic plasticity 4 followed by genetic assimilation, but these processes are often difficult to distinguish in 5 slowly changing environments. This difficulty can be overcome by studying adaptation to 6 more abrupt environmental changes, such as the dramatic transition from life on the Earth's 7 surface to subterranean voids and caves. 8 A unifying feature of subterranean environments is complete darkness (1,2). Cave-adapted 9 animals have evolved a range of unusual and specialized traits, often called troglomorphic 10 traits, which enable survival in challenging conditions of the subsurface. In cave dwelling 11 animals, visual senses and protection from the effects of sunlight are unnecessary, and 12 consequently eyes and pigmentation are usually reduced or absent. To compensate for lack 13 of vision, other traits, especially those related to chemo-and mechano-receptor sensations, 14 are enhanced. Circadian rhythms that fine-tune organismal physiology with day-night cycles 15 are also distorted, and light dependent behaviors, as well as the neural and endocrine 16 circuits controlling these behaviors, are modified. Because photosynthetic organisms are not 17 present in caves, primary productivity is absent and nutrient availability is usually limited. 18 Survival under conditions of reduced and/or sporadic food resources is possible due to the 19 evolution of modified feeding behaviors and adaptive changes in metabolism, such as lower 20 metabolic rate, increased starvation resistance, and changes in carbohydrate and lipid 21 metabolism (1). 22 The ancestors of cave dwelling animals originally lived on the surface. Regardless of whether 23 the pioneering animals entered the subsurface accidently (by capture of surface waters or by 24 falling int...
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