Cave organisms occupy a special place in evolutionary biology because convergent morphologies of many species demonstrate repeatability in evolution even as they obscure phylogenetic relationships. The origin of specialized cave-dwelling species also raises the issue of the relative importance of isolation vs. natural selection in speciation. Two alternative hypotheses describe the origin of subterranean species. The 'climate-relict' model proposes allopatric speciation after populations of cold-adapted species become stranded in caves due to climate change. The 'adaptive-shift' model proposes parapatric speciation driven by divergent selection between subterranean and surface habitats. Our study of the Tennessee cave salamander complex shows that the three nominal forms (Gyrinophilus palleucus palleucus, G. p. necturoides, and G. gulolineatus) arose recently and are genealogically nested within the epigean (surface-dwelling) species, G. porphyriticus. Short branch lengths and discordant gene trees were consistent with a complex history involving gene flow between diverging forms. Results of coalescent-based analysis of the distribution of haplotypes among groups reject the allopatric speciation model and support continuous or recurrent genetic exchange during divergence. These results strongly favour the hypothesis that Tennessee cave salamanders originated from spring salamanders via divergence with gene flow.
In light of recent alarming trends in human population growth, climate change, and other environmental modifications, a “Warning to humanity” manifesto was published in BioScience in 2017. This call reiterated most of the ideas originally expressed by the Union of Concerned Scientists in 1992, including the fear that we are “pushing Earth's ecosystems beyond their capacities to support the web of life.” As subterranean biologists, we take this opportunity to emphasize the global importance and the conservation challenges associated with subterranean ecosystems. They likely represent the most widespread nonmarine environments on Earth, but specialized subterranean organisms remain among the least documented and studied. Largely overlooked in conservation policies, subterranean habitats play a critical role in the function of the web of life and provide important ecosystem services. We highlight the main threats to subterranean ecosystems and propose a set of effective actions to protect this globally important natural heritage.
A major challenge facing biodiversity conservation and management is that a significant portion of species diversity remains undiscovered or undescribed. This is particularly evident in subterranean animals in which species delimitation based on morphology is difficult because differentiation is often obscured by phenotypic convergence. Multilocus genetic data constitute a valuable source of information for species delimitation in such organisms, but until recently, few methods were available to objectively test species delimitation hypotheses using genetic data. Here, we use recently developed methods for discovering and testing species boundaries and relationships using a multilocus dataset in a widely distributed subterranean teleost fish, Typhlichthys subterraneus, endemic to Eastern North America. We provide evidence that species diversity in T. subterraneus is currently underestimated and that the picture of a single, widely distributed species is not supported. Rather, several morphologically cryptic lineages comprise the diversity in this clade, including support for the recognition of T. eigenmanni. The high number of cryptic species in Typhlichthys highlights the utility of multilocus genetic data in delimiting species, particularly in lineages that exhibit slight morphological disparity, such as subterranean organisms. However, results depend on sampling of individuals and loci; this issue needs further study.
It is often hoped that population genetics can answer questions about the demographic and geographic dynamics of recent biological invasions. Conversely, invasions with well-known histories are sometimes billed as opportunities to test methods of population genetic inference. In both cases, underappreciated limitations constrain the usefulness of genetic methods. The most significant is that humancaused invasions have occurred on historical timescales that are orders of magnitude smaller than the timescales of mutation and genetic drift for most multicellular organisms. Analyses based on the neutral theory of molecular evolution cannot resolve such rapid dynamics. Invasion histories cannot be reconstructed in the same way as biogeographic changes occurring over millenia. Analyses assuming equilibrium between mutation, drift, gene flow, and selection will rarely be applicable, and even methods designed for explicitly non-equilibrium questions often require longer timescales than the few generations of most invasions of current concern. We identified only a few population genetic questions that are tractable over such short timescales. These include comparison of alternative hypotheses for the geographic origin of an invasion, testing for bottlenecks, and hybridization between native and invasive species. When proposing population genetic analysis of a biological invasion, we recommend that biologists ask (i) whether the questions to be addressed will materially affect management practice or policy, and (ii) whether the proposed analyses can really be expected to address important population genetic questions. Despite our own enthusiasm for population genetic research, we conclude that genetic analysis of biological invasions is justified only under exceptional circumstances.
The genetic mechanisms underlying regressive evolution-the degeneration or loss of a derived trait-are largely unknown, particularly for complex structures such as eyes in cave organisms. In several eyeless animals, the visual photoreceptor rhodopsin
Using species distribution data, we developed a georeferenced database of troglobionts (cave-obligate species) in Tennessee to examine spatial patterns of species richness and endemism, including >2000 records for 200 described species. Forty aquatic troglobionts (stygobionts) and 160 terrestrial troglobionts are known from caves in Tennessee, the latter having the greatest diversity of any state in the United States. Endemism was high, with 25% of terrestrial troglobionts (40 species) and 20% of stygobionts (eight species) known from just a single cave and nearly two-thirds of all troglobionts (130 species) known from five or fewer caves. Species richness and endemism were greatest in the Interior Plateau (IP) and Southwestern Appalachians (SWA) ecoregions, which were twice as diverse as the Ridge and Valley (RV). Troglobiont species assemblages were most similar between the IP and SWA, which shared 59 species, whereas the RV cave fauna was largely distinct. We identified a hotspot of cave biodiversity with a center along the escarpment of the Cumberland Plateau in south-central Tennessee defined by both species richness and endemism that is contiguous with a previously defined hotspot in northeastern Alabama. Nearly half (91 species) of Tennessee’s troglobiont diversity occurs in this region where several cave systems contain ten or more troglobionts, including one with 23 species. In addition, we identified distinct troglobiont communities across the state. These communities corresponded to hydrological boundaries and likely reflect past or current connectivity between subterranean habitats within and barriers between hydrological basins. Although diverse, Tennessee’s subterranean fauna remains poorly studied and many additional species await discovery and description. We identified several undersampled regions and outlined conservation and management priorities to improve our knowledge and aid in protection of the subterranean biodiversity in Tennessee.
Five decades ago, a landmark paper in Science titled The Cave Environment heralded caves as ideal natural experimental laboratories in which to develop and address general questions in geology, ecology, biogeography, and evolutionary biology. Although the ‘caves as laboratory’ paradigm has since been advocated by subterranean biologists, there are few examples of studies that successfully translated their results into general principles. The contemporary era of big data, modelling tools, and revolutionary advances in genetics and (meta)genomics provides an opportunity to revisit unresolved questions and challenges, as well as examine promising new avenues of research in subterranean biology. Accordingly, we have developed a roadmap to guide future research endeavours in subterranean biology by adapting a well‐established methodology of ‘horizon scanning’ to identify the highest priority research questions across six subject areas. Based on the expert opinion of 30 scientists from around the globe with complementary expertise and of different academic ages, we assembled an initial list of 258 fundamental questions concentrating on macroecology and microbial ecology, adaptation, evolution, and conservation. Subsequently, through online surveys, 130 subterranean biologists with various backgrounds assisted us in reducing our list to 50 top‐priority questions. These research questions are broad in scope and ready to be addressed in the next decade. We believe this exercise will stimulate research towards a deeper understanding of subterranean biology and foster hypothesis‐driven studies likely to resonate broadly from the traditional boundaries of this field.
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