Article
To read the full-text of this research, you can request a copy directly from the authors.

Abstract

Only few fish species have successfully colonized subterranean habitats, but the underlying biological constraints associated with this are still poorly understood. Here, we investigated the influence of permanent darkness on spinal-column development in one species (Midas cichlid, Amphilophus citrinellus) with no known cave form, and one (Atlantic molly, Poecilia mexicana) with two phylogenetically young cave forms. Specifically, fish were reared under a normal light : dark cycle or in permanent darkness (both species). We also surveyed wild-caught cave and surface ecotypes of P. mexicana. In both species, permanent darkness was associated with significantly higher rates of spinal deformities (especially in A. citrinellus). This suggests strong developmental (intrinsic) constraints on the successful colonization of subterranean environments in teleost fishes and might help explain the relative paucity of cave-adapted lineages. Our results add depth to our understanding of the aspects of selection driving trait divergence and maintaining reproductive isolation in cave faunas.

No full-text available

Request Full-text Paper PDF

To read the full-text of this research,
you can request a copy directly from the authors.

... Various body and skeletal deformities in fish have been reviewed in many publications [7][8][9][10][11][12][13][14][15][16]; earlier reports can also be found in Dawson's bibliographies [17][18][19][20]. Many of these deformities apparently can be treated as monstrosities, particularly when the vertebral column is shortened without pronounced curvature, resulting in an altered body form that is extremely short and deep. ...
Article
Full-text available
The phenomenon of a massive vertebral deformity was recorded in the radiating Labeobarbus assemblage from the middle reaches of the Genale River (south-eastern Ethiopia, East Africa). Within this sympatric assemblage, five trophic morphs—generalized, lipped, piscivorous and two scraping feeders—were reported between 1993 and 2019. In 2009, a new morph with prevalence of ~10% was discovered. The new morph, termed ‘short’, had an abnormally shortened vertebral column and a significantly deeper body. This type of deformity is common in farmed Atlantic salmon and other artificially reared fish, but is rare in nature. In the Genale Labeobarbus assemblage, the deformity was present exclusively within the generalized and lipped morphs. The short morph had between seven and 36 deformed (compressed and/or fused) vertebrae. Their body depth was positively correlated with number of deformed vertebrae. In another collection in 2019, the short morph was still present at a frequency of 11%. Various environmental and genetic factors could contribute to the development of this deformity in the Genale Labeobarbus , but based on the available data, it is impossible to confidently identify the key factor(s). Whether the result of genetics, the environment, or both, this deep-bodied phenotype is assumed to be an anti-predator adaptation, as there is evidence of its selective advantage in the generalized morph. The Genale monstrosity is the first reported case of a massive deformity of the vertebral column in a natural population of African fishes.
... 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 dark-raised A. mexicanus SF, Chica CF, and Los Sabinos CF (Rasquin, 1949). 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 (Riesch et al., 2016;Riesch et al., 2011;Torres-Dowdall et al., 2018). Although our study was unable to replicate the changes in body shape seen by Rasquin (1949), we confirmed her observation of increased body fat. ...
Article
Full-text available
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.
... 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 dark-raised A. mexicanus SF, Chica CF, and Los Sabinos CF (Rasquin, 1949). 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 (Riesch et al., 2016;Riesch et al., 2011;Torres-Dowdall et al., 2018). Although our study was unable to replicate the changes in body shape seen by Rasquin (1949), we confirmed her observation of increased body fat. ...
Article
Full-text available
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.
... 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]. ...
Article
Full-text available
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 sul-fide springs. In this paper, we described a new fish species of the genus Jenynsia, Anablepi-dae, 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.
... 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 dark-raised A. mexicanus SF, Chica CF, and Los Sabinos CF (Rasquin, 1949). 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 (Riesch et al., 2016;Riesch et al., 2011;Torres-Dowdall et al., 2018). Although our study was unable to replicate the changes in body shape seen by Rasquin (1949), we confirmed her observation of increased body fat. ...
Preprint
Full-text available
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 .
... Spinal deformities are a frequent phenomenon in many different fish species and can be caused by many factors during fish development, such as bacterial and parasitic infections, water environment, elevated egg incubation temperatures, pollution, nutrients, inappropriate light regimes and vaccination, etc. [2][3][4][5][6][7]. Spinal deformities often result in increased metabolic costs in the deformed fish, leading to reduced growth and low harvest weight [8]. ...
Article
Full-text available
Dwarfism is a condition defined by low harvest weight in fish, but also results in strange body figures which may have potential for the selective breeding of new ornamental fish strains. The objectives of this study are to reveal the physiological causes of dwarfism and identify the genetic loci controlling this trait in the white sailfin molly. Skeletons of dwarf and normal sailfin mollies were observed by X-ray radioscopy and skeletal staining. Genome-wide association studies based on genotyping-by-sequencing (n = 184) were used to map candidate genomic regions associated with the dwarfism trait. Quantitative real-time PCR was performed to determine the expression level of candidate genes in normal (n = 8) and dwarf (n = 8) sailfin mollies. We found that the dwarf sailfin molly has a short and dysplastic spine in comparison to the normal fish. Two regions, located at NW_015112742.1 and NW_015113621.1, were significantly associated with the dwarfism trait. The expression level of three candidate genes, ADAMTS like 1, Larp7 and PPP3CA, were significantly different between the dwarf and normal sailfin mollies in the hepatopancreas, with PPP3CA also showing significant differences in the vertebrae and Larp7 showing significant differences in the muscle. This study identified genomic regions and candidate genes associated with the dwarfism trait in the white sailfin molly and would provide a reference to determine dwarf-causing variations.
... 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 (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. ...
Article
During early ontogeny, visual opsin gene expression in cichlids is influenced by prevailing light reg-imen. 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.
Chapter
The subterranean environment comprises voids of any size in which life can develop in aphotic, aseasonal and largely oligotrophic conditions. A small proportion of living organisms have been able to evolve and adapt to such conditions. Some of them have become strictly dependent on this harsh environment, at the price of a set of profound biological adaptations. Key new discoveries shed light on ancient biogeographical patterns but challenge our views regarding the origin and history of the extant fauna, as illustrated by the recently discovered monospecific genus Iberotrechodes in a cave in Cantabria, Spain. Vicariance by plate tectonics remains the main explanatory factor for the amphi‐Atlantic distribution displayed by many groups of subterranean Crustacea. An accurate knowledge of subterranean diversity at the species level, combined with a comprehensive overview of the geological and paleoclimatic histories of the areas of interest, is a prerequisite to the understanding of biogeographic patterns.
Article
Full-text available
Extreme environmental conditions, such as temperature, can lead to meristic trait variation and skeletal deformities, which may have major impacts on individual fitness. As intertidal ecosystems experience rapid temperature and physicochemical fluctuations, intertidal fish living and reproducing in these environmental conditions may have phenotypes influenced by such variable environments. The impact of intertidal variability on fish development, however, has not been previously investigated. Skeletal deformities and meristic traits were assessed for Bathygobius cocosensis, a common intertidal fish living across the Indo‐Pacific region, using a clearing and staining method on 72 individuals. Over 87% of individuals presented meristic variation and over 70% exhibited at least one type of skeletal deformity, mostly recorded in the caudal fin area. The unexpected prevalence of skeletal deformities among this intertidal fish population suggests that such deformities may be suitable markers to evaluate an individual's stress exposure during development and the subsequent fitness effects.
Article
Full-text available
The anomalies in fish fall into two main categories: severe ones that affect their fitness, and less severe ones that don’t impact survival and may occur as a result of various external and internal factors. Abnormally developed fish can be used as indicators of water pollution because of their high incidence in polluted areas. The objectives of the present study were to report and describe for the first time severe cases of scoliosis and fin deformities in fish from Saudi Arabia. Morphological anomalies, in general, can reduce the weight of fish and, more importantly, impact the value per kg sold. Therefore, the fisheries industries should conduct research into the various etiological causes of the deformities before any management policy can be chosen.
Article
Full-text available
Background Replicate population pairs that diverge in response to similar selective regimes allow for an investigation of (a) whether phenotypic traits diverge in a similar and predictable fashion, (b) whether there is gradual variation in phenotypic divergence reflecting variation in the strength of natural selection among populations, (c) whether the extent of this divergence is correlated between multiple character suites (i.e., concerted evolution), and (d) whether gradual variation in phenotypic divergence predicts the degree of reproductive isolation, pointing towards a role for adaptation as a driver of (ecological) speciation. Here, we use poeciliid fishes of the genera Gambusia and Poecilia that have repeatedly evolved extremophile lineages able to tolerate high and sustained levels of toxic hydrogen sulfide (H2S) to answer these questions. Results We investigated evolutionary divergence in response to H2S in Gambusia spp. (and to a lesser extent Poecilia spp.) using a multivariate approach considering the interplay of life history, body shape, and population genetics (nuclear miscrosatellites to infer population genetic differentiation as a proxy for reproductive isolation). We uncovered both shared and unique patterns of evolution: most extremophile Gambusia predictably evolved larger heads and offspring size, matching a priori predictions for adaptation to sulfidic waters, while variation in adult life histories was idiosyncratic. When investigating patterns for both genera (Gambusia and Poecilia), we found that divergence in offspring-related life histories and body shape were positively correlated across populations, but evidence for individual-level associations between the two character suites was limited, suggesting that genetic linkage, developmental interdependencies, or pleiotropic effects do not explain patterns of concerted evolution. We further found that phenotypic divergence was positively correlated with both environmental H2S-concentration and neutral genetic differentiation (a proxy for gene flow). Conclusions Our results suggest that higher toxicity exerts stronger selection, and that divergent selection appears to constrain gene flow, supporting a scenario of ecological speciation. Nonetheless, progress toward ecological speciation was variable, partially reflecting variation in the strength of divergent selection, highlighting the complexity of selective regimes even in natural systems that are seemingly governed by a single, strong selective agent. Electronic supplementary material The online version of this article (doi:10.1186/s12862-016-0705-1) contains supplementary material, which is available to authorized users.
Article
Full-text available
Caecieleotris morrisi, new genus and species of sleeper (family Eleotridae), is described from a submerged freshwater cave in a karst region of the northern portion of the State of Oaxaca, Mexico, Río Papaloapan drainage, Gulf of Mexico basin. The new species represents the first cave-adapted sleeper known from the Western Hemisphere and is one of only 13 stygobitic gobiiforms known worldwide, with all others limited in distribution to the Indo-Pacific region. The new taxon represents a third independent evolution of a hypogean lifestyle in sleepers, the others being two species of Oxyeleotris (O. caeca and O. colasi) from New Guinea and a single species, Bostrychus microphthalmus, from Sulawesi. Caecieleotris morrisi, new species, is distinguished from epigean eleotrids of the Western Atlantic in lacking functional eyes and body pigmentation, as well as having other troglomorphic features. It shares convergent aspects of morphology with cave-dwelling species of Oxyeleotris and B. microphthalmus but differs from those taxa in lacking cephalic pores and head squamation, among other characters. Description of C. morrisi, new species, brings the total number of eleotrid species known from Mexico to 12. Seven of these, including the new species, occur on the Atlantic Slope. © 2016 by the American Society of Ichthyologists and Herpetologists.
Article
Full-text available
Cavefishes have long been used as model organisms showcasing adaptive diversification, but does adaptation to caves also facilitate the evolution of reproductive isolation from surface ancestors? We raised offspring of wild-caught surface- and cave-dwelling ecotypes of the neotropical fish Poecilia mexicana to sexual maturity in a 12-month common garden experiment. Fish were raised under one of two food regimes (high vs. low), and this was crossed with differences in lighting conditions (permanent darkness vs. 12:12 h light:dark cycle) in a 2 × 2 factorial design, allowing us to elucidate potential patterns of local adaptation in life histories. Our results reveal a pattern of sex-specific local life-history adaptation: Surface molly females had the highest fitness in the treatment best resembling their habitat of origin (high food and a light:dark cycle), and suffered from almost complete reproductive failure in darkness, while cave molly females were not similarly affected in any treatment. Males of both ecotypes, on the other hand, showed only weak evidence for local adaptation. Nonetheless, local life- history adaptation in females likely contributes to ecological diversification in this system and other cave animals, further supporting the role of local adaptation due to strong divergent selection as a major force in ecological speciation.
Article
Full-text available
Background Central American crater lake cichlid fish of the Midas species complex (Amphilophus spp.) are a model system for sympatric speciation and fast ecological diversification and specialization. Midas cichlids have been intensively analyzed from an ecological and morphological perspective. Genomic resources such as transcriptomic and genomic data sets, and a high-quality draft genome are available now. Many ecologically relevant species- specific traits and differences such as pigmentation and cranial morphology arise during development. Detailed descriptions of the early development of the Midas cichlid in particular, will help to investigate the ontogeny of species differences and adaptations. Results We describe the embryonic and larval development of the crater lake cichlid, Amphilophus xiloaensis, until seven days after fertilization. Similar to previous studies on teleost development, we describe six periods of embryogenesis - the zygote, cleavage, blastula, gastrula, segmentation, and post-hatching period. Furthermore, we define homologous stages to well-described teleost models such as medaka and zebrafish, as well as other cichlid species such as the Nile tilapia and the South American cichlid Cichlasoma dimerus. Key  morphological differences between the embryos of Midas cichlids and other teleosts are highlighted and discussed, including the presence of adhesive glands and different early melanophore patterns, as well as variation in developmental timing. Conclusions The developmental staging of the Midas cichlid will aid researchers in the comparative investigation of teleost ontogenies. It will facilitate comparative developmental biological studies of Neotropical and African cichlid fish in particular. In the past, the species flocks of the African Great Lakes have received the most attention from researchers, but some lineages of the 300–400 species of Central American lakes are fascinating model systems for adaptive radiation and rapid phenotypic evolution. The availability of genetic resources, their status as a model system for evolutionary research, and the possibility to perform functional experiments including transgenesis makes the Midas cichlid complex a very attractive model for evolutionary-developmental research.
Article
Full-text available
Background Planarians are an attractive model organism for studying stem cell-based regeneration due to their ability to replace all of their tissues from a population of adult stem cells. The molecular toolkit for planarian studies currently includes the ability to study gene function using RNA interference (RNAi) and observe gene expression via in situ hybridizations. However, there are few antibodies available to visualize protein expression, which would greatly enhance analysis of RNAi experiments as well as allow further characterization of planarian cell populations using immunocytochemistry and other immunological techniques. Thus, additional, easy-to-use, and widely available monoclonal antibodies would be advantageous to study regeneration in planarians.ResultsWe have created seven monoclonal antibodies by inoculating mice with formaldehyde-fixed cells isolated from dissociated 3-day regeneration blastemas. These monoclonal antibodies can be used to label muscle fibers, axonal projections in the central and peripheral nervous systems, two populations of intestinal cells, ciliated cells, a subset of neoblast progeny, and discrete cells within the central nervous system as well as the regeneration blastema. We have tested these antibodies using eight variations of a formaldehyde-based fixation protocol and determined reliable protocols for immunolabeling whole planarians with each antibody. We found that labeling efficiency for each antibody varies greatly depending on the addition or removal of tissue processing steps that are commonly used for in situ hybridization or immunolabeling techniques. Our experiments show that a subset of the antibodies can be used alongside markers commonly used in planarian research, including anti-SYNAPSIN and anti-SMEDWI, or following whole-mount in situ hybridization experiments.Conclusions The monoclonal antibodies described in this paper will be a valuable resource for planarian research. These antibodies have the potential to be used to better understand planarian biology and to characterize phenotypes following RNAi experiments. In addition, we present alterations to fixation protocols and demonstrate how these changes can increase the labeling efficiencies of antibodies used to stain whole planarians.
Article
Full-text available
To describe the occurrence of various spinal deformations in a captive-bred wild line of Poecilia wingei (P. wingei). Fish belonging to a wild line of P. wingei caught from Laguna de Los Patos, Venezuela, were bred in an aquarium home-breeding system during a period of three years (2006-2009). The spinal curvature was observed to study spinal deformities in P. wingei. Out of a total of 600 fish, 22 showed different types of deformities (scoliosis, lordosis, kyphosis), with a higher incidence in females. Growth, swimming and breeding of deformed fish were generally normal. Possible causes for spinal curvature in fish are discussed on the basis of the current literature. While it is not possible to determine the exact cause(s) of spinal deformities observed in the present study, traumatic injuries, nutritional imbalances, genetic defects or a combination of these factors can be supposed to be involved in the pathogenesis of such lesions.
Article
Full-text available
Caves and other subterranean habitats represent one of the most challenging environments on the planet. Other than salamanders, bony fishes are the only vertebrate group that has successfully colonized and are completely restricted to those habitats. Despite being known to science for over 150 years, only recently have cavefishes become model systems for evolutionary studies. Several cavefishes, such as the Mexican characid Astyanax mexicanus, have provided valuable insights into how fishes have evolved to cope with life in perpetual darkness and often-limited food resources. Much less is known about the biology of other cavefishes and their sensory modalities. Here, we summarize the current understanding of nonvisual sensory modalities in cavefishes. Enhancement of mechanosensation appears to be the most common adaptive strategy, but little is known of other sensory modalities in these fishes. Only comparative studies nested within well-resolved phylogenies will clarify the sensory adaptation of fishes to subterranean habitats.
Article
Full-text available
The critical swimming speed (Ucrit, cm s−1) value of normal juvenile sea bass (Dicentrarchus labrax) (64.7±6.33) was significantly higher than that of fish with lordosis (60.3±6.66) (P<0.05). Both normal fish and those with lordosis showed increased endurance with increasing length during exercise at a fixed water velocity of 50 cm s−1. This speed was used to investigate the separation possibility of deformed specimen from the normal developed fish based on their swimming performance, and 28% separation was achieved without losing any normal fish by the end of the 10th minute. To achieve a better separation of the deformities from the normal, first grading of the juveniles and then a swimming endurance test is advised.
Article
Full-text available
Fish store large quantities of vitamin D in their liver and fat tissues, including the fat associated with muscle, and this makes fish an important dietary source of vitamin D. Fish do not synthesize vitamin D and are fully dependent on dietary sources to meet their requirement. Under natural circumstances planktonic vitamin D accumulates in the aquatic food chain. In aquaculture, formulated diets are used and vitamin D intake can be manipulated. The minimum dietary requirement for vitamin D has been established in several fish species. The role of vitamin D in fish physiology is still enigmatic. Till the 1970s there was consensus that fish accumulate but not metabolize vitamin D. There is substantial evidence now, four decades later, that fish have a vitamin D endocrine system with similar functions as in mammals. We here summarize the major characteristics of the fish vitamin D endocrine system. The hydroxylation of vitamin D to more polar metabolites, their plasma levels and protein-bound transport in blood plasma will be discussed. The vitamin D receptor profile, receptor distribution and responses to vitamin D are reviewed for the key target tissues (gill, intestine, kidney and bone). We will address the classical slower actions through transcription factors as well as the faster G-protein coupled (membrane) receptor mediated effects. We then review the dietary requirement of vitamin D in aquaculture and address some lesser known functions of the vitamin D endocrine system.
Article
Full-text available
Background: Closely related lineages of livebearing fishes have independently adapted to two extreme environmental factors: toxic hydrogen sulphide (H(2)S) and perpetual darkness. Previous work has demonstrated in adult specimens that fish from these extreme habitats convergently evolved drastically increased head and offspring size, while cave fish are further characterized by reduced pigmentation and eye size. Here, we traced the development of these (and other) divergent traits in embryos of Poecilia mexicana from benign surface habitats ("surface mollies") and a sulphidic cave ("cave mollies"), as well as in embryos of the sister taxon, Poecilia sulphuraria from a sulphidic surface spring ("sulphur mollies"). We asked at which points during development changes in the timing of the involved processes (i.e., heterochrony) would be detectible. Methods and results: Data were extracted from digital photographs taken of representative embryos for each stage of development and each type of molly. Embryo mass decreased in convergent fashion, but we found patterns of embryonic fat content and ovum/embryo diameter to be divergent among all three types of mollies. The intensity of yellow colouration of the yolk (a proxy for carotenoid content) was significantly lower in cave mollies throughout development. Moreover, while relative head size decreased through development in surface mollies, it increased in both types of extremophile mollies, and eye growth was arrested in mid-stage embryos of cave mollies but not in surface or sulphur mollies. Conclusion: Our results clearly demonstrate that even among sister taxa convergence in phenotypic traits is not always achieved by the same processes during embryo development. Furthermore, teleost development is crucially dependent on sufficient carotenoid stores in the yolk, and so we discuss how the apparent ability of cave mollies to overcome this carotenoid-dependency may represent another potential mechanism explaining the lack of gene flow between surface and cave mollies.
Article
Full-text available
Divergent selection through biotic factors like predation or parasitism can promote reproductive isolation even in the absence of geographical barriers. On the other hand, evidence for a role of adaptation to abiotic factors during ecological speciation in animals is scant. In particular, the role played by perpetual darkness in establishing reproductive isolation in cave animals (troglobites) remains elusive. We focused on two reproductively isolated ecotypes (surface- and cave-dwelling) of the widespread livebearer Poecilia mexicana, and raised offspring of wild-caught females to sexual maturity in a 12-month common-garden experiment. Fish were reared in light or darkness combined with high- or low-food conditions. Females, but not males, of the surface ecotype suffered from almost complete reproductive failure in darkness, especially in the low-food treatment. Furthermore, surface fish suffered from a significantly higher rate of spontaneous, stress-related infection with bacterial columnaris disease. This experimental evidence for strong selection by permanent darkness on non-adapted surface-dwelling animals adds depth to our understanding of the selective forces establishing and maintaining reproductive isolation in cave faunas.
Article
Full-text available
The evolution of degenerate characteristics remains a poorly understood phenomenon. Only recently has the identification of mutations underlying regressive phenotypes become accessible through the use of genetic analyses. Focusing on the Mexican cave tetra Astyanax mexicanus, we describe, here, an analysis of the brown mutation, which was first described in the literature nearly 40 years ago. This phenotype causes reduced melanin content, decreased melanophore number, and brownish eyes in convergent cave forms of A. mexicanus. Crosses demonstrate non-complementation of the brown phenotype in F(2) individuals derived from two independent cave populations: Pachón and the linked Yerbaniz and Japonés caves, indicating the same locus is responsible for reduced pigmentation in these fish. While the brown mutant phenotype arose prior to the fixation of albinism in Pachón cave individuals, it is unclear whether the brown mutation arose before or after the fixation of albinism in the linked Yerbaniz/Japonés caves. Using a QTL approach combined with sequence and functional analyses, we have discovered that two distinct genetic alterations in the coding sequence of the gene Mc1r cause reduced pigmentation associated with the brown mutant phenotype in these caves. Our analysis identifies a novel role for Mc1r in the evolution of degenerative phenotypes in blind Mexican cavefish. Further, the brown phenotype has arisen independently in geographically separate caves, mediated through different mutations of the same gene. This example of parallelism indicates that certain genes are frequent targets of mutation in the repeated evolution of regressive phenotypes in cave-adapted species.
Book
Caves and other subterranean habitats with their often strange (even bizarre) inhabitants have long been objects of fascination, curiosity, and debate. The question of how such organisms have evolved, and the relative roles of natural selection and genetic drift, has engaged subterranean biologists for decades. Indeed, these studies continue to inform the general theory of adaptation and evolution. Subterranean ecosystems generally exhibit little or no primary productivity and, as extreme ecosystems, provide general insights into ecosystem function. The Biology of Caves and other Subterranean Habitats offers a concise but comprehensive introduction to cave ecology and evolution. Whilst there is an emphasis on biological processes occurring in these unique environments, conservation and management aspects are also considered. The monograph includes a global range of examples from more than 25 countries, and case studies from both caves and non-cave subterranean habitats; it also provides a clear explanation of specialized terms used by speleologists. This accessible text will appeal to researchers new to the field and to the many professional ecologists and conservation practitioners requiring a concise but authoritative overview. Its engaging style will also make it suitable for undergraduate and graduate students taking courses in cave and subterranean biology. Its more than 650 references, 150 of which are new since the first edition, provide many entry points to the research literature.
Article
During early ontogeny, visual opsin gene expression in cichlids is influenced by prevailing light reg-imen. 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.
Article
Caves and other associated subterranean habitats represent some of the most challenging environments on Earth. Despite many significant abiotic and biotic obstacles to overcome, most notably the complete absence of light, several groups of fishes thrive in subterranean habitats. The aim of this chapter is to provide a broad yet thorough review of our current knowledge regarding fish adaptations to one of the most extreme habitats on the planet. We begin our chapter by providing an overview of subterranean habitats, focusing on caves, and the major constraints cavefishes must overcome to live in such environments in complete darkness with limited food resources. We then provide an overview of taxonomic diversity and geographic distribution of cavefishes with a brief discussion of syntopy of cavefishes in subterranean habitats. Next we summarize what is known about the physiological, behavioral, and morphological adaptations that have evolved in cavefishes in response to the primary physicochemical and ecological stressors in subterranean habitats. In particular, we focus on adaptations associated with nonvisual sensory modalities. Finally, we offer a few suggestions for avenues of future research in cavefish adaptation and sensory evolution.
Article
South America harbours the most diverse freshwater fish fauna in the world, and recent estimates point to between 6000 and 8000 species in the Neotropical region. Such fauna has diverse historical origins, either having invaded and diversified in fresh water from marine ancestors during the Palaeogene or being isolated on the continent since the end of the break-up of Gondwana in the Cretaceous. Taxonomic, morphological and ecological diversity of South American freshwater fishes is dramatic, as are the myriad freshwater habitats they inhabit. Unfortunately, many of these habitats are severely threatened by deforestation, water divergence for irrigation, industry and other uses by humans, hydroelectric damming, mining, pollution and invasive species. Despite these multiple threats, there are very few on-the-ground conservation initiatives in South America, although assessments of species-extinction risks have been produced at regional and subregional levels in different countries.
Article
The purpose of the present study was to investigate the effect of vitamin D3 compounds on the occurrence of hypermelanosis on the blind side and vertebral deformity in juvenile Japanese flounder Paralichthys olivaceus . To elucidate the mechanism by which vitamin D 3 causes hypermelanosis in Japanese flounder, larvae (total length (TL), 9.8 ± 0.77 mm; 22 days post-hatching (dph)) were fed an artificial diet without any vitamin D supplement control group), a diet supplemented with 0.5 mg vitamin D 3 /100 g (VD 3 group), or a diet supplemented with 0.05 mg 1,25-dihydroxyvitamin D 3 /100 g (1,25(OH)2D3 group) until 49 dph. Fish were harvested at 49 dph and 70 dph for assessment of the TL, survival, igmentation, and vertebral deformity. A high incidence of hypermelanosis on the blind side was observed on the head and caudal regions in all groups at both 49 dph and 70 dph. A significantly higher frequency of occurrence of severe hypermelanosis on the trunk region of the blind side was observed in the 1,25(OH)2D3 group (P <0.05) compared with the control group at 70 dph. Moreover, completely hyperpigmented fish were observed only in the 1,25(OH)2D3 group. A higher frequency of the occurrence of winding of the abdominal vertebrae was also observed in the VD3 and 1,25(OH)2D3 groups (P<0.05).
Article
Chronic environmental stress is known to induce evolutionary change. Here, we assessed male life-history trait divergence in the neotropical fish Poecilia mexicana from a system that has been described to undergo incipient ecological speciation in adjacent, but reproductively isolated toxic/nontoxic and surface/cave habitats. Examining both field-caught and common garden-reared specimens, we investigated the extent of differentiation and plasticity of life-history strategies employed by male P. mexicana. We found strong site-specific life-history divergence in traits such as fat content, standard length and gonadosomatic index. The majority of site-specific life-history differences were also expressed under common garden-rearing conditions. We propose that apparent conservatism of male life histories is the result of other (genetically based) changes in physiology and behaviour between populations. Together with the results from previous studies, this is strong evidence for local adaptation as a result of ecologically based divergent selection.
Article
How cave animals adapt to life in darkness is a poorly understood aspect of evolutionary biology [1]. Here we identify a behavioral shift and its morphological basis in Astyanax mexicanus, a teleost with a sighted surface-dwelling form (surface fish) and various blind cave-dwelling forms (cavefish) [2-4]. Vibration attraction behavior (VAB) is the ability of fish to swim toward the source of a water disturbance in darkness. VAB was typically seen in cavefish, rarely in surface fish, and was advantageous for feeding success in the dark. The potential for showing VAB has a genetic component and is linked to the mechanosensory function of the lateral line. VAB was evoked by vibration stimuli peaking at 35 Hz, blocked by lateral line inhibitors, first detected after developmental increases in superficial neuromast (SN) number and size [5-7], and significantly reduced by bilateral ablation of SN. We conclude that VAB and SN enhancement coevolved to compensate for loss of vision and to help blind cavefish find food in darkness.
Article
Life-history traits are very sensitive to extreme environmental conditions, because resources that need to be invested in somatic maintenance cannot be invested in reproduction. Here we examined female life-history traits in the Mexican livebearing fish Poecilia mexicana from a variety of benign surface habitats, a creek with naturally occurring toxic hydrogen sulfide (H2S), a sulfidic cave, and a non-sulfidic cave. Previous studies revealed pronounced genetic and morphological divergence over very small geographic scales in this system despite the absence of physical barriers, suggesting that local adaptation to different combinations of two selection factors, toxicity (H2S) and darkness, is accompanied by very low rates of gene flow. Hence, we investigated life-history divergence between these populations in response to the selective pressures of darkness and/or toxicity. Our main results show that toxicity and darkness both select for (or impose constraints on) the same female trait dynamics: reduced fecundity and increased offspring size. Since reduced fecundity in the sulfur cave population was previously shown to be heritable, we discuss how divergent life-history evolution may promote further ecological divergence: for example, reduced fecundity and increased offspring autonomy are clearly beneficial in extreme environments, but fish with these traits are outcompeted in benign habitats.
Article
Melatonin is a much conserved feature in vertebrates that plays a central role in the entrainment of daily and annual physiological rhythms. Investigations aiming at understanding how melatonin mediates the effects of photoperiod on crucial functions and behaviors have been very active in the last decades, particularly in mammals. In fish a clear-cut picture is still missing. Here we review the available data on (i) the sites of melatonin production in fish, (ii) the mechanisms that control its daily and annual rhythms of production and (iii) the characterization of its different receptor subtypes, their location and regulation. The in vivo and in vitro data on melatonin effects on crucial neuroendocrine regulations, including reproduction, growth, feeding and behavioral responses, are also reviewed. Finally we discuss how manipulation of the photic cues impact on fish circannual clock and annual cycle of reproduction, and how this can be used for aquaculture purposes. Request by email to get a copy of the article
Article
This study addresses the role of sonic hedgehog (shh) in increasing oral-pharyngeal constructive traits (jaws and taste buds) at the expense of eyes in the blind cavefish Astyanax mexicanus. In cavefish embryos, eye primordia degenerate under the influence of hyperactive Shh signaling. In concert, cavefish show amplified jaw size and taste bud numbers as part of a change in feeding behavior. To determine whether pleiotropic effects of hyperactive Shh signaling link these regressive and constructive traits, shh expression was compared during late development of the surface-dwelling (surface fish) and cave-dwelling (cavefish) forms of Astyanax. After an initial expansion along the midline of early embryos, shh was elevated in the oral-pharyngeal region in cavefish and later was confined to taste buds. The results of shh inhibition and overexpression experiments indicate that Shh signaling has an important role in oral and taste bud development. Conditional overexpression of an injected shh transgene at specific times in development showed that taste bud amplification and eye degeneration are sensitive to shh overexpression during the same early developmental period, although taste buds are not formed until much later. Genetic crosses between cavefish and surface fish revealed an inverse relationship between eye size and jaw size/taste bud number, supporting a link between oral-pharyngeal constructive traits and eye degeneration. The results suggest that hyperactive Shh signaling increases oral and taste bud amplification in cavefish at the expense of eyes. Therefore, selection for constructive oral-pharyngeal traits may be responsible for eye loss during cavefish evolution via pleiotropic function of the Shh signaling pathway.
Article
The physiological function of vitamin D in fishes still remains uncertain. Earlier we observed no relationship between vitamin D3 content of several freshwater fishes and their calcemic/phosphatemic status and bone mineral content. In the present study the effects of vitamin D3 and its metabolites, 25-hydroxy vitamin D3 (25-OH-D3) and 1,25-dihydroxy vitamin D3 [1,25-(OH)2D3], administration on serum calcium-phosphorus levels, intestinal calcium absorption, whole-body calcium-phosphorus uptake, and gill calcium binding protein (CaBP) activity in the freshwater fish, Tilapia mossambica (Tilapia) was examined. It was observed that vitamin D3 and its metabolites could alter neither serum calcium-phosphorus levels nor intestinal calcium absorption and gill CaBP activity in fish at various doses. Further, the whole-body uptake of labelled calcium and phosphorus was also unaffected by vitamin D3/1,25-(OH)2D3 at different levels and/or at various lengths of time. Thus these studies indicate that unlike in terrestrial vertebrates, vitamin D3 or its metabolites are not needed for calcium-phosphorus homeostasis in fish.
Article
Vertebral development is a dynamic and complicated process, and defects can be caused by a variety of influences. Spinal curvature with no known cause (idiopathic scoliosis) affects 2-3% of the human population. In order to understand the etiology and pathogenesis of complex human skeletal defects such as idiopathic scoliosis, multiple models must be used to study all of the factors affecting vertebral stability and deformity. Although fish and humans have many of the same types of offenses to vertebral integrity, they have been overlooked as a resource for study. The most common morphological deformity reported for fish are those that occur during the development of the spinal system, and as with humans, curvature is a common morphological consequence. Here we review spinal curvature in teleosts and suggest that they are an unexploited resource for understanding the basic elements of vertebral stability, deformity, development and genetics. Fish can be a value to vertebral research because they are tractable, have a diversity of non-induced vertebral deformities, and substantial genomic resources. Current animal models lack non-induced deformities and the experimental tractability necessary for genetic studies. The fact that fish are free of an appendicular skeleton should allow for analysis of basic spinal integrity without the biomechanical constraints observed in quadrupedal and bipedal models. To illustrate the point we review human idiopathic scoliosis and the potential contribution teleosts can make for the identification of causes, risk factors, and treatment options.
Survey of North American cave vertebrates
  • Dearolf K
Dearolf K. 1956 Survey of North American cave vertebrates. Proc. Pa Acad. Sci. 30, 201-210.