Evolution in caves: selection from darkness causes spinal deformities in teleost fishes

Torres‐Dowdall, Julián; Karagic, Nidal; Plath, Martin; Riesch, Rüdiger

doi:10.1098/rsbl.2018.0197

Cited by 14 publications

(10 citation statements)

References 26 publications

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“…We expected to find plastic changes in D/D reared SF involving pituitary and thyroid hormonal regulation, adipose tissue, and body shape based on the previous work on darkraised A. mexicanus SF, Chica CF, and Los Sabinos CF [47]. Furthermore, experiments on Poecillia mexicana, another teleost with cave adapted lineages, showed that darkness caused degenerate changes in the spine and promoted sexual isolation between adjacent surface and cave lineages [50][51][52]. Although our study was unable to replicate the changes in body shape seen by Rasquin (1949), we confirmed her observation of the increase of body fat.…”

Section: Discussionmentioning

confidence: 98%

Phenotypic plasticity as a mechanism of cave colonization and adaptation

Bilandžija

Hollifield

Steck

et al. 2019

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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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Section: Discussionmentioning

confidence: 98%

Phenotypic plasticity as a mechanism of cave colonization and adaptation

Bilandžija

Hollifield

Steck

et al. 2019

Preprint

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“…Development of DD individuals was decelerated compared with LD individuals and the developmental lag increased over time and malformations of the spine accumulated (Figure 1). Several studies on fish under reduced illumination (Bolla & Holmefjord, 1988;Villamizar et al, 2011;Torres-Dowdall, Karagic, Plath, & Riesch, 2018). One potential explanation for the developmental lag in Midas cichlids is the inability to capture food in the dark environment.…”

Section: Development Is Decelerated In Dark-reared Midas Cichlidsmentioning

confidence: 99%

Heterochronic opsin expression due to early light deprivation results in drastically shifted visual sensitivity in a cichlid fish: Possible role of thyroid hormone signaling

et al. 2018

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During early ontogeny, visual opsin gene expression in cichlids is influenced by prevailing light regimen. Red light, for example, leads to an early switch from the expression of short-wavelength sensitive to long-wavelength sensitive opsins. Here, we address the influence of light deprivation on opsin expression. Individuals reared in constant darkness during the first 14 days post-hatching (dph) showed a general developmental delay compared with fish reared under a 12:12 hr light-dark cycle (control group). Several characters including pigmentation patterns and eye development, appeared later in dark-reared individuals. Quantitative real-time PCR and fluorescent in situ hybridization at six time points during the 14 days period revealed that fish from the control group expressed opsin genes from 5 dph on and maintained a short-wavelength sensitive phenotype (sws1, rh2b, and rh2a). Onset of opsin expression in dark-reared Midas cichlids was delayed by 4 days and visual sensitivity rapidly progressed toward a long-wavelength sensitive phenotype (sws2b, rh2a, and lws). Shifts in visual sensitivities toward longer wavelengths are mediated by thyroid hormone (TH) in many vertebrates. Compared to control fish, dark-reared individuals showed elevated dio3 expression levels - a validated proxy for TH concentration - suggesting higher circulating TH levels. Despite decelerated overall development, ontogeny of opsin gene expression was accelerated, resulting in retinae with long-wavelength shifted predicted sensitivities compared to light-reared individuals. Indirect evidence suggests that this was due to altered TH metabolism.

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“…Extremophile species inhabiting environments with abiotic conditions lethal for most organisms, are of great interest to physiologists, ecologists and evolutionary biologists [1, 2]. These species offer valuable information on the limits of tolerance to abiotic conditions (e.g., [3]), on the process of adaptive divergence (e.g, [4]), and in the end, about the predictability of evolution (e.g., [5]). In fact, species inhabiting extreme ecological conditions have provided some very interesting cases of evolutionary convergence at different levels of biological organization, from molecular changes, to physiology, morphology, and performance [6, 7].…”

Section: Introductionmentioning

confidence: 99%

Molecular and morphological convergence to sulfide-tolerant fishes in a new species of Jenynsia (Cyprinodontiformes: Anablepidae), the first extremophile member of the family

et al. 2019

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Freshwater sulfide springs have extreme environmental conditions that only few vertebrate species can tolerate. These species often develop a series of morphological and molecular adaptations to cope with the challenges of life under the toxic and hypoxic conditions of sulfide springs. In this paper, we described a new fish species of the genus Jenynsia , Anablepidae, from a sulfide spring in Northwestern Argentina, the first in the family known from such extreme environment. Jenynsia sulfurica n. sp. is diagnosable by the lack of scales on the pre-pelvic area or the presence of a single row of scales, continuous or not, from the isthmus to the bases of the pelvic fins. Additionally, it presents a series of morphological and molecular characteristics that appear convergent with those seen in other fish species (e.g., Poeciliids) inhabiting sulfide springs. Most notably, J . sulfurica has an enlarged head and postorbital area compared to other fish of the genus and a prognathous lower jaw with a hypertrophied lip, thought to facilitate respiration at the air-water interface. Analyses of cox1 sequence showed that J . sulfurica has two unique mutations resulting in amino acid substitutions convergent to those seen in Poeciliids from sulfide springs and known to provide a physiological mechanism related to living in sulfide environments. A phylogenetic analysis, including molecular and morphological characters, placed J . sulfurica as sister taxa to J . alternimaculata , a species found in nearby, non-sulfide habitats directly connected to the sulfide springs. Thus, it can be inferred that the selection imposed by the presence of H 2 S has resulted in the divergence between these two species and has potentially served as a barrier to gene flow.

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Evolution in caves: selection from darkness causes spinal deformities in teleost fishes

Cited by 14 publications

References 26 publications

Phenotypic plasticity as a mechanism of cave colonization and adaptation

Phenotypic plasticity as a mechanism of cave colonization and adaptation

Heterochronic opsin expression due to early light deprivation results in drastically shifted visual sensitivity in a cichlid fish: Possible role of thyroid hormone signaling

Molecular and morphological convergence to sulfide-tolerant fishes in a new species of Jenynsia (Cyprinodontiformes: Anablepidae), the first extremophile member of the family

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