Quantitative Aspekte der regressiven Evolution – dargestellt am Beispiel der Augenrückbildung bei Höhlenfischen

Quantitative aspects of regressive evolution – demonstrated by the reduction of the eyes in cave fishes According to our present understanding, the eyes of cave fishes are no longer subject to a stabilizing selection. Because of a strong mutation pressure in the destructive direction, this leads to a continual enrichment of elimination mutants and thereby to a progressive reduction of the eyes after separation of a cave population. Obviously a natural selection process does not play a significant role in the reduction of the eyes in cave fishes. Based on these findings, the degeneration process can be characterized in detail, especially concerning its course and duration.     

Cave-adapted evolution in the North American amblyopsid fishes inferred using phylogenomics and geometric morphometrics

Cave adaptation has evolved repeatedly across the Tree of Life, famously leading to pigmentation and eye degeneration and loss, yet its macroevolutionary implications remain poorly understood. We use the North American amblyopsid fishes, a family spanning a wide degree of cave adaptation, to examine the impact of cave specialization on the modes and tempo of evolution. We reconstruct evolutionary relationships using ultraconserved element loci, estimate the ancestral histories of eye-state, and examine the impact of cave adaptation on body shape evolution. Our phylogenomic analyses provide a well-supported hypothesis for amblyopsid evolutionary relationships. The obligate blind cavefishes form a clade and the cave-facultative eyed spring cavefishes are nested within the obligate cavefishes. Using ancestral state reconstruction, we find support for at least two independent subterranean colonization events within the Amblyopsidae. Eyed and blind fishes have different body shapes, but not different rates of body shape evolution. North American amblyopsids highlight the complex nature of cave-adaptive evolution and the necessity to include multiple lines of evidence to uncover the underlying processes involved in the loss of complex traits.     

Sex recognition in surface- and cave-dwelling Atlantic molly females (<Emphasis Type="Italic">Poecilia mexicana</Emphasis>, Poeciliidae,Teleostei): influence of visual and non-visual cues

Cave fishes need to rely on non-visual senses, such as the sense of smell or the lateral line to communicate in darkness. In the present study, we investigated sex identification by females of a cave-dwelling livebearing fish, Poecilia mexicana (cave molly), as well as its surface-dwelling relatives. Unlike many other cave fishes, cave mollies still possess functional eyes. Three different modes of presentation of the stimulus fish (a male and an equally sized female) were used: (i) the stimulus fish were presented behind wire-mesh in light, allowing the focal female to perceive multiple cues, (ii) the experiment was carried out under infrared conditions, such that only non-visual cues could be perceived and (iii) the stimulus fish were presented in light behind transparent Plexiglas, allowing for the use of visual cues only. Females of all populations examined preferred to associate with the stimulus female in at least one of the treatments, but only when visible light was provided, suggesting that far-range sex recognition is limited or even absent in the cave molly under naturally dark conditions.     

Nontroglobitic Fishes in Bruffey-Hills Creek Cave, West Virginia, and other Caves Worldwide

Six species of fishes were tagged and released in September and November 1995 and on five dates between November 1998 and October 1999 inside Bruffey-Hills Creek Cave. Most of the tagged fishes were creek chub, Semotilus atromaculatus, and green sunfish, Lepomis cyanellus. The overall recapture rate was 2.6% as only three of 117 fishes were recaptured. Forty-nine days was the longest time of residence by two L. cyanellus and one S. atromaculatus, and movement of 83.4 m was observed only for the creek chub. Tag loss was confirmed as one factor in the low recapture rate. Nine species of fishes were collected in the cave, including Phoxinus oreas and Pimephales promelas, two species never collected in a cave. Most of the fishes were pigmented normally, but many creek chubs were depigmented and appeared white or pigmentless when first observed in the cave stream. Four species, Phoxinus oreas, Pimephales promelas, Ameiurus nebulosus, and Lepomis macrochirus, were collected for the first time in Bruffey-Hills Creek Cave and in the Bruffey and Hills creeks drainage. Although data from this study did not shed light on residence time of fishes in the cave, the consistent occurrence of epigean fishes in this cave was shown. A list of epigean fishes from caves worldwide was included along with a discussion of aspects of the ecology of epigean fishes in caves and of evolution of troglobitic fishes.     

Responses to light in two blind cave fishes (Amblyopsis spelaea and Typhlichthys subterraneus) (Pisces: Amblyopsidae)

Explanations for the phenotypical features resulting from colonization of subterranean environments have always been a source of controversy. Although a great number of cave organisms are blind, they nevertheless display responses to light. The interpretation of this phototactic responsiveness in cave-dwelling animals may provide clues on the general issue of evolution of behavior in parallel with specialized structures. We studied the phototactic responses in two amblyopsid fishes of North America and found responses to light only in the species reported to have a functional pineal organ. Our findings are consistent with the hypotheses that (1) adaptation to the cave environment is a gradual process and (2) responsiveness to light in cave fishes may best be understood as a relict character, one that exists in an environment where it may never be expressed.     

Predation of a cave fish (Poecilia mexicana, Poeciliidae) by a giant water-bug (Belostoma, Belostomatidae) in a Mexican sulphur cave

Abstract.  1. Caves are often assumed to be predator-free environments for cave fishes. This has been proposed to be a potential benefit of colonising these otherwise harsh environments. In order to test this hypothesis, the predator–prey interaction of a belostomatid (predator) and a cave fish (prey) occurring in the Cueva del Azufre (Tabasco, Mexico) was investigated with two separate experiments.
2. In one experiment, individual Belostoma were given a chance to prey on a cave fish, the cave form of the Atlantic molly ( Poecilia mexicana ), to estimate feeding rates and size-specific prey preferences of the predator. In the other experiment, population density of Belostoma was estimated using a mark–recapture analysis in one of the cave chambers.
3. Belostomatids were found to heavily prey on cave mollies and to exhibit a prey preference for large fish. The mark–recapture analysis revealed a high population density of the heteropterans in the cave.
4. The absence of predators in caves is not a general habitat feature for cave fishes. None the less predation regimes differ strikingly between epigean and hypogean habitats. The prey preference of Belostoma indicates that cave-dwelling P. mexicana experience size-specific predation pressure comparable with surface populations, which may have implications for life-history evolution in this cave fish.     

Parallel evolution leads to reduced shoaling behavior in two cave dwelling populations of Atlantic mollies (<Emphasis Type="Italic">Poecilia mexicana</Emphasis>, Poeciliidae,Teleostei)

Shoaling behavior protects fishes from avian and piscine predation, but at the same time costs of group living arise due to several mechanisms including increased food competition. Most cave fishes live in an environment in which avian and piscine predators are lacking, and cave environments are often characterized by low food availability, leading to increased food competition. Altogether, this should favor the reduction of shoaling in cave fishes. We compared shoaling behavior (i.e. the tendency to associate with a stimulus shoal) among surface dwelling populations of the Atlantic molly, Poecilia mexicana, and two cave forms of that species. The first cave population of P. mexicana originated from the Cueva del Azufre and was previously recognized as the only cave form of a poeciliid fish. The second cave population examined came from a cave that was discovered only recently (Cueva Luna Azufre). In both cave forms shoaling behavior was reduced compared with surface dwelling mollies.     

Nucleotide diversity in populations of balitorid cave fishes from Thailand

Genetic variabilities in four cave and eight surface species of balitorid freshwater fishes from Thailand were assessed using random amplified polymorphic DNA (RAPD). Cave species have consistently lower RAPD variation than surface species and it is hypothesized that this difference is a function of reduced population size in cave fishes. Indices of nucleotide diversity (pi) were calculated from the RAPD data and are four to five times higher for the surface species than the cave species: 6.4 x 10-3 vs. 1.4 x 10-3. The pi-values for cave fishes are significantly lower than those for surface balitorids and those measured in other species using RAPD/amplified fragment length polymorphism data.     

Adaptations of Cave Fishes with some Comparisons to Deep-sea Fishes

I provide my retrospective and prospective views on adaptations of cave fishes. I emphasize the history of my insights into cave adaptation from 45 years of research using surface, cave-spring, and cave species of amblyopsid fishes. My approach has been to use natural experiments and to always consider multiple hypotheses. To clarify evolutionary adaptations, I show the importance of a broad comparative approach which includes studies of morphology, metabolic physiology, foraging behavior, life history, and ecology. And I show that the most important agents of selection, of darkness and attendant low food supply, are best understood in the context of rigor, variability, and predictability. I also present my insights from what I consider the most insightful contributions on deep-sea fishes. The contributions are those of Marshall in studies of morphology in relation to energy economy of pelagic and benthic species, Childress in studies of physiological and biochemical adaptations with depth for pelagic species, and Koslow in studies on population biology and life history of bathybenthic and benthic sea-mount species. Compared to caves, I suggest that the extremes of metabolic and life history adaptations of deep-sea fish are explained by a longer evolutionary history and a much greater habitat range, food supply, and predation risk. Finally, I take a retrospective view of what we have learned about cave fishes. I discuss possible evolutionary mechanisms that can explain the trends with increasing cave adaptation in amblyopsid fishes, especially progenesis and the pleiotropic effects of the stress resistance syndrome. Finally, based on insights from deep-sea fishes, and emerging new techniques, I suggest what cave fish biologists should do in the future.     

The end of regressive evolution: examining and interpreting the evidence from cave fishes

The evolution of hypogean fauna in general and hypogean fishes in particular has been controversial. Explanations regarding the reduction or loss of phenotypic characters such as eyes and pigmentation range from neo‐Lamarckism to neutral mutations, with 'regressive evolution' being a catch‐all characterization for such processes. The assumptions required for special evolutionary mechanisms underlying the evolution of cave dwellers have been based on generalizations about the animals and their environments drawn from relatively few observations. The evidence offered for notions such as pre‐adaptation of colonizing fauna and the purported impoverished nutrients in all caves is examined and it appears that the generalizations cannot be supported. Some major accomplishments in field and laboratory studies of hypogean fishes are summarized, including work highlighting developmental phenotypic plasticity. At the end, it is argued that evolution of hypogean fauna can be explained by well‐known mechanisms within the current context of evolutionary biology.     

Developmental constraints in regressive evolution: studies of the expression of the γs-crystallin gene in the developing lens of cave-dwelling Astyanax fasciatus (Cuvier, 1819) (Teleostei, Characidae) by in situ hybridization

The early morphogenesis of the lens and the expression of the γs-crystallin gene was studied in epigean Astyanax fasciatus and its cave-dwelling derivative. At early stages, the lens of the cave fish develops in a way that is similar to the epigean form. Later, the developmental timing is delayed and growth ceases in the cave-fish lens. With the beginning of cytodifferentiation, the development of the lens breaks down. Crystallin lens fibres are not produced at any time and the γs-crystallin gene, which is transcribed during a limited period in the lens of epigean fishes, is not active in cave specimens. This study confirms earlier immunofluorescence observations that demonstrated the lack of crystallin proteins in the cave-fish lens, but is in contrast to results on the blind mole rat, which showed a persistence of functioning crystallins in the degenerated lens of this species. The significance of developmental constraints in regressive evolution is discussed.     

Relaxed purifying selection of rhodopsin gene within a Chinese endemic cavefish genus <Emphasis Type="Italic">Sinocyclocheilus</Emphasis> (Pisces: Cypriniformes)

The cyprinid fish genus Sinocyclocheilus, as the most cavefish rich genus, includes many species showing striking adaptation to caves and convergent reduction or even loss of eyes and pigmentation. RH1 is responsible for dim vision. In order to explore the evolution of RH1 gene in this genus, we sequenced the complete gene from 28 individuals of 16 representative species of Sinocyclocheilus, with cave and surface species included. Phylogenetic analyses supported the monophyly of Sinocyclocheilus and polyphyly of the cave species. Codon models implemented in PAML were used to infer the evolution of RH1. We found that Sinocyclocheilus had a significantly higher evolutionary rate for amino acids than other cyprinid fishes compared, which might be the result of relaxation of purifying selection and could be ascribed to cave habit of this genus. In contrast to previous hypotheses, both cave and surface lineages exhibited a similar rate of molecular evolution, so the RH1 of cave species may still be functional, although these species were highly adapted to cave environment. Two amino acid substitutions (D83G and E122V) that were not reported before were found, which may be useful for site-directed mutagenesis in the future. Handling editor: Christian Sturmbauer     

By the teeth of their skin, cavefish find their way

Teeth and skin teeth (denticles), collectively named odontodes, are usually associated with the physical roles of cutting, protection or drag reduction in fishes [1,2]. These structures are composed of a soft pulp surrounded by dentine and covered by a mineralized substance such as enamel [3]. Odontodes arise from neural crest cells and epithelium and are often innervated [1-3]. However, little is known about their possible sensory function. Here, we demonstrate for the first time a mechanosensory role for denticles in a cavefish endemic to a fast water flow cave. All fishes gather hydrodynamic information via specialized sense organs called neuromasts [4-6]. Some fishes are especially attentive to such type of information [5] and until now hypertrophy of the neuromast system has been reported as the main constructive sensory adaptation in cavefishes [6,7]. We expect that the mechanosensory nature of denticles highlighted in this cave fish species might reflect a widespread sensory role for these structures in other animals.     

Phylogenetic perspectives in the evolution of parental care in ray-finned fishes

Among major vertebrate groups, ray-finned fishes (Actinopterygii) collectively display a nearly unrivaled diversity of parental care activities. This fact, coupled with a growing body of phylogenetic data for Actinopterygii, makes these fishes a logical model system for analyzing the evolutionary histories of alternative parental care modes and associated reproductive behaviors. From an extensive literature review, we constructed a supertree for ray-finned fishes and used its phylogenetic topology to investigate the evolution of several key reproductive states including type of parental care (maternal, paternal, or biparental), internal versus external fertilization, internal versus external gestation, nest construction behavior, and presence versus absence of sexual dichromatism (as an indicator of sexual selection). Using a comparative phylogenetic approach, we critically evaluate several hypotheses regarding evolutionary pathways toward parental care. Results from maximum parsimony reconstructions indicate that all forms of parental care, including paternal, biparental, and maternal (both external and internal to the female reproductive tract) have arisen repeatedly and independently during ray-finned fish evolution. The most common evolutionary transitions were from external fertilization directly to paternal care and from external fertilization to maternal care via the intermediate step of internal fertilization. We also used maximum likelihood phylogenetic methods to test for statistical correlations and contingencies in the evolution of pairs of reproductive traits. Sexual dichromatism and nest construction proved to be positively correlated with the evolution of male parental care in species with external fertilization. Sexual dichromatism was also positively correlated with female-internal fertilization and gestation. No clear indication emerged that female-only care or biparental care were evolutionary outgrowths of male-only care, or that biparental care has been a common evolutionary stepping stone between paternal and maternal care. Results are discussed in the context of prior thought about the evolution of alternative parental care modes in vertebrates.     

Out of sight out of mind: current knowledge of Chinese cave fishes

Caves and karsts are among the most threatened ecosystems in the world. They are very fragile, balanced habitats with high levels of endemic species that are extremely sensitive to environmental changes. In recent decades, however, threats from rapid economic growth have increased the need for conservation efforts for cave-dwelling communities. In addition, difficulties in accessing and sampling these habitats mean that they remain as one of the least known ecosystems in the world with modern studies of cave fishes only starting in China during the 1980s. Here, the current status of cave fishes in China is reviewed. China is host to the highest number of cave fish species in the world, with 48 troglobite species out of a total of 101 cave fish species. All of these cave fish species (one order and three families) and half of the genera are endemic to China with Sinocyclocheilus being the most speciose cave fish genus. Species from this genus possess horns and humpbacks resulting from processes of parallel evolution, but the function of these features remains unknown. With the exception of Onychostoma macrolepis distributed in north China, all other species are found in the karst environment of the Yunnan-Guizhou Plateau. Sympatric distribution is common, and sometimes several different cave fish species can be found in the same cave or subterranean river. For this reason, Chinese cave fishes represent an important evolutionary framework.     

洞穴鱼类:概念、多样性及研究进展

洞穴鱼类是淡水鱼类中一个特殊的生态类群,其生活史的自然完成离不开洞穴或地下水环境。洞穴鱼类可分为典型和非典型两种类型,前者具有易辨识的特殊适应性形态结构(如眼消失、身体透明等),后者此类特征不明显。目前世界典型洞穴鱼类共记录有107种,其中鲤形目和鲇形目的种类最多,分别占49.5%和24.3%;在科级水平上以鲤科和爬鳅科最为丰富。东南亚和中南美是洞穴鱼类多样性最高的地区,有着世界上75.0%的典型洞穴鱼类。中国的洞穴鱼类具有物种多样性高、但集中出现在个别类群(如金线鲃属(Sinocyclocheilus)和高原鳅属(Triplophysa))、物种分化强烈、分布范围狭窄、种群数量小等特点。洞穴鱼类学是一门交叉科学,研究涉及系统学、生态学、生理学、保护生物学等众多学科领域,但目前研究仍多围绕演化问题展开。中国洞穴鱼类研究还处于系统分类和区系研究水平,其他有关学科的研究有待开展。     

Rates of deleterious mutation and the evolution of sex in Caenorhabditis

A variety of models propose that the accumulation of deleterious mutations plays an important role in the evolution of breeding systems. These models make predictions regarding the relative rates of protein evolution and deleterious mutation in taxa with contrasting modes of reproduction. Here we compare available coding sequences from one obligately outcrossing and two primarily selfing species of Caenorhabditis to explore the potential for mutational models to explain the evolution of breeding system in this clade. If deleterious mutations interact synergistically, the mutational deterministic hypothesis predicts that a high genomic deleterious mutation rate (U) will offset the reproductive disadvantage of outcrossing relative to asexual or selfing reproduction. Therefore, C. elegans and C. briggsae (both largely selfing) should both exhibit lower rates of deleterious mutation than the obligately outcrossing relative C. remanei. Using a comparative approach, we estimate U to be equivalent (and < 1) among all three related species. Stochastic mutational models, Muller's ratchet and Hill-Robertson interference, are expected to cause reductions in the effective population size in species that rarely outcross, thereby allowing deleterious mutations to accumulate at an elevated rate. We find only limited support for more rapid molecular evolution in selfing lineages. Overall, our analyses indicate that the evolution of breeding system in this group is unlikely to be explained solely by available mutational models.     

A Novel Role for Mc1r in the Parallel Evolution of Depigmentation in Independent Populations of the Cavefish Astyanax mexicanus

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 F₂ 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.     

On the karyosystematics of cyprinid fishes and a summary of fish chromosome studies in China

To date, the chromosomes of 210 species of fresh-water fishes have been studied in China. They are principally cyprinids. Based upon the karyotypic data so far obtained mainly by the authors' laboratory, a report is here submitted on the karyosystematics of Chinese cyprinid fishes.The primitive karyotype of cyprinid fishes may be inferred as being 2n=50. During phyletic evolution the cyprinid fishes probably have been differentiated into two large branches, one of which with the Leuciscinae as a basic group and another branch with the Barbinae as a basic group. As to the modes of their chromosome evolution, Robertsonian translocation seems to be prominent in the first branch, whereas polyploidization appears to be prominent in the second branch. Based on the chromosome studies in cyprinid fishes, some tentative ideas about the classification of the subfamilies in Cyprinidae are presented.A table containing the karyotypes of Chinese fresh-water fishes is attached.This work was partially supported by the Science Fund of the Chinese Academy of Science.     

Life on the edge: hydrogen sulfide and the fish communities of a Mexican cave and surrounding waters

Most eucaryotic organisms classified as living in an extreme habitat are invertebrates. Here we report of a fish living in a Mexican cave (Cueva del Azufre) that is rich in highly toxic H₂S. We compared the water chemistry and fish communities of the cave and several nearby surface streams. Our study revealed high concentrations of H₂S in the cave and its outflow (El Azufre). The concentrations of H₂S reach more than 300 μM inside the cave, which are acutely toxic for most fishes. In both sulfidic habitats, the diversity of fishes was heavily reduced, and Poecilia mexicana was the dominant species indicating that the presence of H₂S has an all-or-none effect, permitting only few species to survive in sulfidic habitats. Compared to habitats without H₂S, P. mexicana from the cave and the outflow have a significantly lower body condition. Although there are microhabitats with varying concentrations of H₂S within the cave, we could not find a higher fish density in areas with lower concentrations of H₂S. We discuss that P. mexicana is one of the few extremophile vertebrates. Our study supports the idea that extreme habitats lead to an impoverished species diversity.