Evolution in caves: Darwin’s ‘wrecks of ancient life’ in the molecular era

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.     

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.     

Evolution of cave living in Hawaiian Schrankia (Lepidoptera: Noctuidae) with description of a remarkable new cave species

Although temperate cave‐adapted fauna may evolve as a result of climatic change, tropical cave dwellers probably colonize caves through adaptive shifts to exploit new resources. The founding populations may have traits that make colonization of underground spaces even more likely. To investigate the process of cave adaptation and the number of times that flightlessness has evolved in a group of reportedly flightless Hawaiian cave moths, we tested the flight ability of 54 Schrankia individuals from seven caves on two islands. Several caves on one island were sampled because separate caves could have been colonized by underground connections after flightlessness had already evolved. A phylogeny based on approximately 1500 bp of mtDNA and nDNA showed that Schrankia howarthi sp. nov. invaded caves on two islands, Maui and Hawaii. Cave‐adapted adults are not consistently flightless but instead are polymorphic for flight ability. Although the new species appears well suited to underground living, some individuals were found living above ground as well. These individuals, which are capable of flight, suggest that this normally cave‐limited species is able to colonize other, geographically separated caves via above‐ground dispersal. This is the first example of an apparently cave‐adapted species that occurs in caves on two separate Hawaiian islands. A revision of the other Hawaiian Schrankia is presented, revealing that Schrankia simplex, Schrankia oxygramma, Schrankia sarothrura, and Schrankia arrhecta are all junior synonyms of Schrankia altivolans. © 2009 The Linnean Society of London, Zoological Journal of the Linnean Society, 2009, 156 , 114–139.     

Cultivable microscopic fungi from an underground chemosynthesis-based ecosystem: a preliminary study

Movile Cave, a unique groundwater ecosystem in southern Romania, was discovered in 1986. This chemoautotrophic cave contains an abundant and diverse fauna with terrestrial and aquatic invertebrate communities, including 33 endemic species. Since its discovery, studies have focused mainly on cave chemoautotrophic bacteria, while the microfungal community has been largely neglected. In this study, we determined the microfungal species living on various substrates in Movile Cave and compared this spectrum with the mycobiota detected outside the cave (outside air-borne and soil-borne microfungi). To investigate all of the niches, we collected samples for two consecutive years from the dry part of the cave (cave air and sediment, corroded limestone walls, isopod feces, and isopod and spider cadavers) and from the post-siphon part of the cave, i.e., Airbell II (sediment and floating microbial mat). A total of 123 microfungal species were identified from among several hundred isolates. Of these, 96 species were only detected in the cave environment and not outside of the cave, while 90 species were from the dry part of the cave and 28 were from Airbell II. The most diverse genera were Penicillium (at least 18 species) and Aspergillus (14 species), followed by Cladosporium (9 species). Surprisingly, high CFU counts of air-borne microfungi were found inside the cave; they were even higher than outside the cave during the first year of investigation.     

Cyto‐nuclear discordance suggests complex evolutionary history in the cave‐dwelling salamander,Eurycea lucifuga

Our understanding of the evolutionary history and ecology of cave‐associated species has been driven historically by studies of morphologically adapted cave‐restricted species. Our understanding of the evolutionary history and ecology of nonrestricted cave species, troglophiles, is limited to a few studies, which present differing accounts of troglophiles’ relationship with the cave habitat, and its impact on population dynamics. Here, we used phylogenetics, demographic statistics, and population genetic methods to study lineage divergence, dates of divergence, and population structure in the Cave Salamander, Eurycea lucifuga, across its range. In order to perform these analyses, we sampled 233 individuals from 49 populations, using sequence data from three gene loci as well as genotyping data from 19 newly designed microsatellite markers. We find, as in many other species studied in a phylogeographic context, discordance between patterns inferred from mitochondrial relationships and those inferred by nuclear markers indicating a complicated evolutionary history in this species. Our results suggest Pleistocene‐based divergence among three main lineages within E. lucifuga corresponding to the western, central, and eastern regions of the range, similar to patterns seen in species separated in multiple refugia during climatic shifts. The conflict between mitochondrial and nuclear patterns is consistent with what we would expect from secondary contact between regional populations following expansion from multiple refugia.     

Speciation with gene flow in a narrow endemic West Virginia cave salamander (Gyrinophilus subterraneus)

Due to their limited geographic distributions and specialized ecologies, cave species are often highly endemic and can be especially vulnerable to habitat degradation within and surrounding the cave systems they inhabit. We investigated the evolutionary history of the West Virginia Spring Salamander (Gyrinophilus subterraneus), estimated the population trend from historic and current survey data, and assessed the current potential for water quality threats to the cave habitat. Our genomic data (mtDNA sequence and ddRADseq-derived SNPs) reveal two, distinct evolutionary lineages within General Davis Cave corresponding to G. subterraneus and its widely distributed sister species, Gyrinophilus porphyriticus, that are also differentiable based on morphological traits. Genomic models of evolutionary history strongly support asymmetric and continuous gene flow between the two lineages, and hybrid classification analyses identify only parental and first generation cross (F1) progeny. Collectively, these results point to a rare case of sympatric speciation occurring within the cave, leading to strong support for continuing to recognize G. subterraneus as a distinct and unique species. Due to its specialized habitat requirements, the complete distribution of G. subterraneus is unresolved, but using survey data in its type locality (and currently the only known occupied site), we find that the population within General Davis Cave has possibly declined over the last 45 years. Finally, our measures of cave and surface stream water quality did not reveal evidence of water quality impairment and provide important baselines for future monitoring. In addition, our unexpected finding of a hybrid zone and partial reproductive isolation between G. subterraneus and G. porphyriticus warrants further attention to better understand the evolutionary and conservation implications of occasional hybridization between the species.

     

EVOLUTION OF ADULT MORPHOLOGY AND LIFE-HISTORY CHARACTERS IN CAVERNICOLOUS PTOMAPHAGUS BEETLES

Morphological and life-history characters were determined for a series of six increasingly cavernicolous species of eastern United States Ptomaphagus beetles. Contrary to expectations, dimensions of only some adult structural characters uniformly covary as an overall measure of evolutionary adaptation for cave life. Adult reproductive characters that show adaptation for cave life are loss of reproductive seasonality and production of fewer and larger eggs. Significant change in pre-imaginal life-cycle stages was not found. This is in contrast to cavernicolous bathysciine beetles of Europe which show remarkable adaptive trends in pre-imaginal stages, but larval adaptations are not strongly coevolved with adult cave-adaptive characters. This suggests that evolution of cave adaptation in adult endopterygote insects occurs before and independently from that in larvae.     

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.     

北京房山十渡西太平洞晚更新世哺乳动物化石

北京市房山区十渡镇西太平村发现的动物化石是首次在该镇辖区发现的更新世化石。动物群由6目、15科、22属的22种组成,以岩羊、香麝及鼯鼠等为主,为典型的北方山区动物群。该动物群的时代为晚更新世晚期,~(14)C年代为距今29335～37350年,与山顶洞及田园洞动物群基本同期。西太平洞动物群中有76%的种曾出现于周口店田园洞动物群,而只有38%的种曾出现于山顶洞。目前在此发现的可鉴定到种的化石材料均可归入现生种,但其中有23%的种已经在北京地区消失,消失属种以大中型动物为主。在该地点发现的西伯利亚飞鼠和复齿鼯鼠材料是首次在华北地区发现的此类化石记录。该地点是我国北方地区已报道的第四纪化石点中含香麝和岩羊材料最丰富的地点之一。在国内有关文献中,岩羊化石的分类命名一直没有得到统一,这次发现的新材料,有利于澄清该类化石的分类命名问题。     

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.     

Hickmania Troglodytes, the Tasmanian Cave Spider, and its Potential Role in Cave Management

Cave faunas – which often contain a high representation of spiders – are subject to increasing pressure from the effects of epigean habitat degradation and recreational caving activities. Hickmania troglodytes is a prominent member of the Tasmanian cave fauna, a spider of phylogenetic, zoogeographic and ecological importance, but about which little has previously been known. Long-term monitoring has revealed many unusual life-cycle characteristics in this species, most of which occur over long periods of time and are dependent upon environmental stability. The species presents a potentially useful tool in the management and monitoring of cave fauna and karst, as it is large, conspicuous, numerous, ubiquitous, sedentary, functionally significant and potentially sensitive to various sources of disturbance. H. troglodytes may provide a visible and obvious measure of disturbance in and around cave entrances, and may also prove useful in detecting broader scale impacts affecting the entire cave. Many promising developments are being made in terms of cave management in Tasmania, but other issues are less well addressed and still need to be resolved. With further research, the use of indicator or sentinel species may prove to be well suited to the less complex and often sparsely populated subterranean environment, and may play an important role within larger management strategies for cave fauna and karst.     

Reduction in the metabolic levels due to phenotypic plasticity in the Pyrenean newt,Calotriton asper,during cave colonization

According to theories on cave adaptation, cave organisms are expected to develop a lower metabolic rate compared to surface organisms as an adaptation to food scarcity in the subterranean environments. To test this hypothesis, we compared the oxygen consumption rates of the surface and subterranean populations of a surface‐dwelling species, the newt Calotriton asper, occasionally found in caves. In this study, we designed a new experimental setup in which animals with free movement were monitored for several days in a respirometer. First, we measured the metabolic rates of individuals from the surface and subterranean populations, both maintained for eight years in captivity in a natural cave. We then tested individuals from these populations immediately after they were caught and one year later while being maintained in the cave. We found that the surface individuals that acclimated to the cave significantly reduced their oxygen consumption, whereas individuals from the subterranean population maintained in the cave under a light/dark cycle did not significantly modify their metabolic rates. Second, we compared these metabolic rates to those of an obligate subterranean salamander (Proteus anguinus), a surface aquatic Urodel (Ambystoma mexicanum), and a fish species (Gobio occitaniae) as references for surface organisms from different phyla. As predicted, we found differences between the subterranean and surface species, and the metabolic rates of surface and subterranean C. asper populations were between those of the obligate subterranean and surface species. These results suggest that the plasticity of the metabolism observed in surface C. asper was neither directly due to food availability in our experiments nor the light/dark conditions, but due to static temperatures. Moreover, we suggest that this adjustment of the metabolic level at a temperature close to the thermal optimum may further allow individual species to cope with the food limitations of the subterranean environment.     

Chronological and Isotopic data support a revision for the timing of cave bear extinction in Mediterranean Europe

Abstract

The Cave Bear, Ursus spelaeus (sensu lato), was one of many megafaunal species that became extinct during the Late Pleistocene in Europe. With new data we revisit the debate about the extinction and paleoecology of this species by presenting new chronometric, isotopic and taphonomic evidence from two Palaeolithic cave bear sites in northeastern Italy: Paina Cave and Trene Cave. Two direct radiocarbon dates on well-preserved collagen have yielded ages around 24,200–23,500 cal yr BP, which make them the latest known representatives of the species in Europe. The carbon (δ¹³C) and nitrogen (δ¹⁵N) isotopic values of bone collagen exhibit values similar to those of older cave bears from Swabian Jura and France, suggesting that the feedings preferences of cave bears remained unchanged until the disappearance of this species in Europe. Several bear remains preserved traces of human modification such as cut marks, which enables a reconstruction of the main steps of fur recovery and the butchering process. The broad range of plant types available and the favorable location of Berici Hills may have played an important role in the range expansion of cave bears and their interaction with the Paleolithic hunters settled the same area.     

Phylogenetic evidence from freshwater crayfishes that cave adaptation is not an evolutionary dead‐end

Caves are perceived as isolated, extreme habitats with a uniquely specialized biota, which long ago led to the idea that caves are “evolutionary dead‐ends.” This implies that cave‐adapted taxa may be doomed for extinction before they can diversify or transition to a more stable state. However, this hypothesis has not been explicitly tested in a phylogenetic framework with multiple independently evolved cave‐dwelling groups. Here, we use the freshwater crayfish, a group with dozens of cave‐dwelling species in multiple lineages, as a system to test this hypothesis. We consider historical patterns of lineage diversification and habitat transition as well as current patterns of geographic range size. We find that while cave‐dwelling lineages have small relative range sizes and rarely transition back to the surface, they exhibit remarkably similar diversification patterns to those of other habitat types and appear to be able to maintain a diversity of lineages through time. This suggests that cave adaptation is not a “dead‐end” for freshwater crayfish, which has positive implications for our understanding of biodiversity and conservation in cave habitats.     

Surface to subsurface freshwater connections: phylogeographic and habitat analyses of Cambarus tenebrosus, a facultative cave-dwelling crayfish

This study examined the phylogeography and population demographics of Cambarus tenebrosus , which has an unusually large distribution for a freshwater crayfish species, encompassing the Interior Lowlands and Cumberland Plateau of the eastern United States. This facultative cave-dweller provides a unique perspective on the biologic connections between surface and subsurface freshwater ecosystems, which are considered to be highly imperiled due to pollution and habitat degradation. The 16S mitochondrial gene was sequenced for 233 individuals from 84 cave and 20 surface locations throughout the range, with most sampling concentrated around the Cumberland Plateau of the southern Appalachians, to assess conservation status of this species and examine the extent of gene flow between the two habitat types. Cave and surface populations formed a single monophyletic group relative to Cambarus striatus , and clades showed strong geographical associations, but lacked habitat structuring. Occupation of subterranean environments does not appear to be a recent event in the evolutionary history of the species. The large amount of genetic diversity within the species, coupled with its ability to inhabit surface and subsurface environments, suggests that this species may pose a threat as a possible invasive species in other karst-dominated landscapes.     

与南京汤山直立人伴生的偶蹄类及其古环境浅析

在汤山葫芦洞大洞发现的偶蹄类化石共有 4个科、 5个属种 ,其中化石毛冠鹿为首次在华东地区发现。除德氏水牛相似种以外 ,其它属种与周口店第 1地点的标本相比具有个体较大(如李氏野猪、葛氏斑鹿和肿骨鹿 )或形态较进步 (如李氏野猪、似德氏水牛 )。这些动物所反映的古环境为植被丰富 ,并以阔叶乔木和灌木为主 ,间有局部开阔草地。当时的年平均气温与现在相似 ,但冬季偏冷。     

广西崇左泊岳山巨猿洞早更新世的鼠科化石

最近在广西崇左泊岳山巨猿洞采集到大量步氏巨猿、猩猩、长臂猿等高等灵长类及伴生的属种丰富的哺乳动物化石。本文系统记述了该化石点小哺乳动物群中的优势群体——鼠科化石:似锡金小鼠(Mus cf.M.pahari)、似大林姬鼠(Apodemus cf.A.peninsulae)、细狨鼠(Hapalomys gracilis)、狭齿狨鼠(Hapalomys angustidens)、先社鼠(Niviventer preconfucianus)、安氏白腹鼠(Niviventer andersoni)、拟爱氏巨鼠(Leopoldamys edwardsioides)和似始家鼠(Rattus cf.R.pristinus)共6属8种,其中包括了5个绝灭种。研究表明,泊岳山巨猿洞鼠类主要属种的形态特征显然要比同地区的三合大洞显得原始,而较相似于重庆巫山龙骨坡的相关鼠类,因此推测其时代为早更新世早期,这与古地磁的测年结果(距今约180万年)相吻合。泊岳山巨猿洞的鼠类大部分均为东洋界成员以及树栖、半树栖及林地生活的种类,反映当时的自然景观为热带-亚热带的森林-林灌环境。泊岳山巨猿洞鼠科化石的研究丰富了我国南方早更新世巨猿-中华乳齿象动物群中小哺乳动物化石的记录,这对于探讨我国南方第四纪生物地层的划分将提供重要的信息。     

Ancient origin of a Western Mediterranean radiation of subterranean beetles

Background  

Cave organisms have been used as models for evolution and biogeography, as their reduced above-ground dispersal produces phylogenetic patterns of area distribution that largely match the geological history of mountain ranges and cave habitats. Most current hypotheses assume that subterranean lineages arose recently from surface dwelling, dispersive close relatives, but for terrestrial organisms there is scant phylogenetic evidence to support this view. We study here with molecular methods the evolutionary history of a highly diverse assemblage of subterranean beetles in the tribe Leptodirini (Coleoptera, Leiodidae, Cholevinae) in the mountain systems of the Western Mediterranean.