Cave animals have historically attracted the attention of evolutionary biologists because of their bizarre 'regressive' characters and convergent evolution. However, understanding of their ...biogeographic and evolutionary history, including mechanisms of speciation, has remained elusive. In the last decade, molecular data have been obtained for subterranean taxa and their surface relatives, which have allowed some of the classical debates on the evolution of cave fauna to be revisited. Here, we review some of the major studies, focusing on the contribution of phylogeography in the following areas: biogeographic history and the relative roles of dispersal and vicariance, colonization history, cryptic species diversity and modes of speciation of cave animals. We further consider the limitations of current research and prospects for the future. Phylogeographic studies have confirmed that cave species are often cryptic, with highly restricted distributions, but have also shown that their divergence and potential speciation may occur despite the presence of gene flow from surface populations. Significantly, phylogeographic studies have provided evidence for speciation and adaptive evolution within the confines of cave environments, questioning the assumption that cave species evolved directly from surface ancestors. Recent technical developments involving 'next generation' DNA sequencing and theoretical developments in coalescent and population modelling are likely to revolutionize the field further, particularly in the study of speciation and the genetic basis of adaptation and convergent evolution within subterranean habitats. In summary, phylogeographic studies have provided an unprecedented insight into the evolution of these unique fauna, and the future of the field should be inspiring and data rich.
A deep-dive into the evolutionary biology, biogeography, and conservation of the most elusive subterranean creatures in the world.Far from the austere, sparsely populated ecosystems often conjured in ...the imagination, caves host some of the most mysterious and biodiverse natural systems in the world. Subterranean environments, however, are the least explored terrestrial habitats, contributing to misconceptions about their inhabitants. Edited by cave scientist and conservation ecologist Dr. J. Judson Wynne, Cave Biodiversity explores both the evolution and the conservation of subterrestrial-dwelling fauna. Covering both vertebrates and invertebrates, including mollusks, fishes, amphibians, arthropods, and other troglobionts, this volume brings together ichthyologists, entomologists, ecologists, herpetologists, and conservationists to provide a nuanced picture of life beneath the earth's surface. Broad chapters covering biotic and abiotic factors that influence evolution and support biodiversity precede chapters dedicated to specific taxa, highlighting phylogenetics and morphology, and delving into zoogeography, habitat, ecology, and dispersal mechanisms for each. Considerations for conservation of these fascinating, often bizarre, and often highly sensitive subterranean creatures are emphasized throughout.Cave Biodiversity aims to synthesize the principles of subterranean evolutionary biology and diversity through in-depth case studies of some of the most captivating and imperiled taxonomic groups in the world. Employing a multidisciplinary approach involving systematics, genetics, ecology, biogeography, evolutionary biology, and conservation science, Cave Biodiversity will be of keen interest to evolutionary biologists, ecologists, conservation biologists, and cave scientists, as well as advanced undergraduate and graduate students. Contributors: Maria E. Bichuette, Evin T. Carter, Prosanta Chakrabarty, Kenneth James Chapin, Danté B. Fenolio, Andrew G. Gluesenkamp, Jozef Grego, Francis G. Howarth, Leonardo Latella, Matthew L. Niemiller, Karen A. Ober, T. Keith Philips, John G. Phillips, Stuart Pimm, Daphne Soares, J. Judson Wynne, and Yahui Zhao.
Caves pose significant challenges for mining projects, since they harbor many endemic and threatened species, and must therefore be protected. Recent discussions between academia, environmental ...protection agencies, and industry partners, have highlighted problems with the current Brazilian legislation for the protection of caves. While the licensing process is long, complex and cumbersome, the criteria used to assign caves into conservation relevance categories are often subjective, with relevance being mainly determined by the presence of obligate cave dwellers (troglobites) and their presumed rarity. However, the rarity of these troglobitic species is questionable, as most remain unidentified to the species level and their habitats and distribution ranges are poorly known. Using data from 844 iron caves retrieved from different speleology reports for the Carajás region (South-Eastern Amazon, Brazil), one of the world's largest deposits of high-grade iron ore, we assess the influence of different cave characteristics on four biodiversity proxies (species richness, presence of troglobites, presence of rare troglobites, and presence of resident bat populations). We then examine how the current relevance classification scheme ranks caves with different biodiversity indicators. Large caves were found to be important reservoirs of biodiversity, so they should be prioritized in conservation programs. Our results also reveal spatial autocorrelation in all the biodiversity proxies assessed, indicating that iron caves should be treated as components of a cave network immersed in the karst landscape. Finally, we show that by prioritizing the conservation of rare troglobites, the current relevance classification scheme is undermining overall cave biodiversity and leaving ecologically important caves unprotected. We argue that conservation efforts should target subterranean habitats as a whole and propose an alternative relevance ranking scheme, which could help simplify the assessment process and channel more resources to the effective protection of overall cave biodiversity.
Novel phenotypes can come about through a variety of mechanisms including standing genetic variation from a founding population. Cave animals are an excellent system in which to study the evolution ...of novel phenotypes such as loss of pigmentation and eyes. Asellus aquaticus is a freshwater isopod crustacean found in Europe and has both a surface and a cave ecomorph which vary in multiple phenotypic traits. An orange eye phenotype was previously revealed by F2 crosses and backcrosses to the cave parent within two examined Slovenian cave populations. Complete loss of pigmentation, both in eye and body, is epistatic to the orange eye phenotype and therefore the orange eye phenotype is hidden within the cave populations. Our goal was to investigate the origin of the orange eye alleles within the Slovenian cave populations by examining A. aquaticus individuals from Slovenian and Romanian surface populations and Asellus aquaticus infernus individuals from a Romanian cave population. We found orange eye individuals present in lab raised surface populations of A. aquaticus from both Slovenia and Romania. Using a mapping approach with crosses between individuals of two surface populations, we found that the region known to be responsible for the orange eye phenotype within the two previously examined Slovenian cave populations was also responsible within both the Slovenian and the Romanian surface populations. Complementation crosses between orange eye Slovenian and orange eye Romanian surface individuals suggest that the same gene is responsible for the orange eye phenotype in both surface populations. Additionally, we observed a low frequency phenotype of eye loss in crosses generated between the two surface populations and also in the Romanian surface population. Finally, in a cave population from Romania, A. aquaticus infernus, we found that the same region is also responsible for the orange eye phenotype as the Slovenian cave populations and the Slovenian and Romanian surface populations. Therefore, we present evidence that variation present in the cave populations could originate from standing variation present in the surface populations and/or transgressive hybridization of different surface phylogenetic lineages rather than de novo mutations.
An orange eye phenotype, hidden within cave populations (masked by absence of pigment), was uncovered through crossing cave populations with surface populations. A similar orange eye phenotype can be found within surface populations suggesting that orange alleles within the cave populations originated from standing variation in the founding surface population.
One of the most challenging fauna to study in situ is the obligate cave fauna because of the difficulty of sampling. Cave-limited species display patchy and restricted distributions, but it is often ...unclear whether the observed distribution is a sampling artifact or a true restriction in range. Further, the drivers of the distribution could be local environmental conditions, such as cave humidity, or they could be associated with surface features that are surrogates for cave conditions. If surface features can be used to predict the distribution of important cave taxa, then conservation management is more easily obtained. We examined the hypothesis that the presence of major faunal groups of cave obligate species could be predicted based on features of the earth surface. Georeferenced records of cave obligate amphipods, crayfish, fish, isopods, beetles, millipedes, pseudoscorpions, spiders, and springtails within the area of Appalachian Landscape Conservation Cooperative in the eastern United States (Illinois to Virginia and New York to Alabama) were assigned to 20 x 20 km grid cells. Habitat suitability for these faunal groups was modeled using logistic regression with twenty predictor variables within each grid cell, such as percent karst, soil features, temperature, precipitation, and elevation. Models successfully predicted the presence of a group greater than 65% of the time (mean = 88%) for the presence of single grid cell endemics, and for all faunal groups except pseudoscorpions. The most common predictor variables were latitude, percent karst, and the standard deviation of the Topographic Position Index (TPI), a measure of landscape rugosity within each grid cell. The overall success of these models points to a number of important connections between the surface and cave environments, and some of these, especially soil features and topographic variability, suggest new research directions. These models should prove to be useful tools in predicting the presence of species in understudied areas.
Fish reproductive patterns are very diverse in terms of breeding frequency, mating system, sexual dimorphisms and selection, mate choice, spawning site choice, courtship patterns, spawning behaviors ...and parental care. Here we have compared the breeding behavior of the surface-dwelling and cave-dwelling morphs of the characiform A. mexicanus, with the goals of documenting the spawning behavior in this emerging model organism, its possible evolution after cave colonization, and the sensory modalities involved. Using infrared video recordings, we showed that cave and surface Astyanax spawning behavior is identical, occurs in the dark, and can be divided into 5 rapid phases repeated many times, about once per minute, during spawning sessions which last about one hour and involve one female and several males. Such features may constitute "pre-adaptive traits" which have facilitated fish survival after cave colonization, and may also explain how the two morphs can hybridize in the wild and in the laboratory. Accordingly, cross-breeding experiments involving females of one morphotype and males of the other morphotype showed the same behavior including the same five phases. However, breeding between cavefish females and surface fish males was more frequent than the reverse. Finally, cavefish female pheromonal solution was able to trigger strong behavioral responses in cavefish males-but not on surface fish males. Lastly, egg production seemed higher in surface fish females than in cavefish females. These results are discussed with regards to the sensory modalities involved in triggering reproductive behavior in the two morphs, as well as its possible ongoing evolution.
Telomeres are non-coding DNA repeats at the chromosome ends and their shortening is considered one of the major causes of aging. However, they also serve as a biomarker of environmental exposures and ...their length and attrition is affected by various stressors. In this study, we examined the average telomere length in
, a species that has both surface-dwelling and cave-adapted populations. The cave morph descended from surface ancestors and adapted to a markedly different environment characterized by specific biotic and abiotic stressors, many of which are known to affect telomere length. Our objective was to explore whether telomere length differs between the two morphs and whether it serves as a biological marker of aging or correlates with the diverse environments the morphs are exposed to.
We compared telomere length and shortening between laboratory-reared Pachón cavefish and Rio Choy surface fish of
across different tissues and ages.
surface fish exhibited longer average telomere length compared to cavefish. In addition, we did not observe telomere attrition in either cave or surface form as a result of aging in adults up to 9 years old, suggesting that efficient mechanisms prevent telomere-mediated senescence in laboratory stocks of this species, at least within this time frame. Our results suggest that telomere length in
may be considered a biomarker of environmental exposures. Cavefish may have evolved shorter and energetically less costly telomeres due to the absence of potential stressors known to affect surface species, such as predator pressure and ultra-violet radiation. This study provides the first insights into telomere dynamics in
morphs and suggests that shorter telomeres may have evolved as an adaptation to caves.
The genus Troglocladius Andersen, Baranov et Hagenlund, gen. n. is erected based on T. hajdi Andersen, Baranov et Hagenlund, sp. n. collected at 980 m depth in the Lukina jama-Trojama cave system in ...Croatia. Morphological features such as pale color, strongly reduced eyes and very long legs make it a typical cave animal. Surprisingly, it has also retained large wings and appears to be capable of flight which would make T. hajdi the first flying troglobiont worldwide, disproving previous beliefs that bats are the only animals capable of flying in complete darkness. Morphologically the new species does not readily fit within any described genus, but shares characteristics with genera both in the tribes "Metriocnemini" and "Orthocladiini". Bayesian molecular phylogenetic analysis using the markers COI, 18S rDNAs, 28S rDNA, CADI, and CADIV groups it with the genera Tvetenia, Cardiocladius and Eukiefferiella in the tribe "Metriocnemini". Troglocladius hajdi may be parthenogenetic, as only females were collected. The discovery confirms the position of the Dinaric arch as a highly important hotspot of subterranean biodiversity.
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