Ancient lineage, young troglobites: recent colonization of caves by Nesticella spiders

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Abstract

Background

The evolution and origin of cave organisms is a recurring issue in evolutionary studies, but analyses are often hindered by the inaccessibility of caves, morphological convergence, and complex colonization processes. Here we investigated the evolutionary history of Nesticella cave spiders, which are mainly distributed in the Yunnan–Guizhou Plateau, China. With comprehensive sampling and phylogenetic and coalescent-based analyses, we investigated the tempo and mode of diversification and the origins of these troglobites. We also aimed to determine which factors have influenced the diversification of this little-known group.

Results

Coalescent-based species delimitation validated the 18 species recognized by morphological inspection and also suggested the existence of cryptic lineages. Divergence time estimates suggested that Nesticella cave spiders in the Yunnan–Guizhou Plateau constituted a monophyletic troglobite clade that originated in the middle Miocene (11.1–18.6 Ma). Although the Yunnan–Guizhou Plateau clade was composed exclusively of troglobite species, suggesting an ancient common subterranean ancestor, we favor multiple, independent cave colonizations during the Pleistocene over a single ancient cave colonization event to explain the origin of these cave faunas. The diversification of plateau Nesticella has been greatly influenced by the sequential uplift of the plateau and likely reflects multiple cave colonizations over time by epigean ancestors during Pleistocene glacial advances.

Conclusions

We concluded that plateau cave Nesticella represent an ancient group of spiders, but with young troglobite lineages that invaded caves only recently. The absence of extant epigean relatives and nearly complete isolation among caves supported their relict status. Our work highlights the importance of comprehensive sampling for studies of subterranean diversity and the evolution of cave organisms. The existence of potentially cryptic species and the relict status of Nesticella highlight the need to conserve these cave spiders.

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Most cited references 35

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Bayesian species delimitation using multilocus sequence data.

Ziheng Yang, Bruce Rannala (2010)

In the absence of recent admixture between species, bipartitions of individuals in gene trees that are shared across loci can potentially be used to infer the presence of two or more species. This approach to species delimitation via molecular sequence data has been constrained by the fact that genealogies for individual loci are often poorly resolved and that ancestral lineage sorting, hybridization, and other population genetic processes can lead to discordant gene trees. Here we use a Bayesian modeling approach to generate the posterior probabilities of species assignments taking account of uncertainties due to unknown gene trees and the ancestral coalescent process. For tractability, we rely on a user-specified guide tree to avoid integrating over all possible species delimitations. The statistical performance of the method is examined using simulations, and the method is illustrated by analyzing sequence data from rotifers, fence lizards, and human populations.

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Time dependency of molecular rate estimates and systematic overestimation of recent divergence times.

Simon Y W Ho, Matthew J. Phillips, Alan Cooper … (2005)

Studies of molecular evolutionary rates have yielded a wide range of rate estimates for various genes and taxa. Recent studies based on population-level and pedigree data have produced remarkably high estimates of mutation rate, which strongly contrast with substitution rates inferred in phylogenetic (species-level) studies. Using Bayesian analysis with a relaxed-clock model, we estimated rates for three groups of mitochondrial data: avian protein-coding genes, primate protein-coding genes, and primate d-loop sequences. In all three cases, we found a measurable transition between the high, short-term (< 1-2 Myr) mutation rate and the low, long-term substitution rate. The relationship between the age of the calibration and the rate of change can be described by a vertically translated exponential decay curve, which may be used for correcting molecular date estimates. The phylogenetic substitution rates in mitochondria are approximately 0.5% per million years for avian protein-coding sequences and 1.5% per million years for primate protein-coding and d-loop sequences. Further analyses showed that purifying selection offers the most convincing explanation for the observed relationship between the estimated rate and the depth of the calibration. We rule out the possibility that it is a spurious result arising from sequence errors, and find it unlikely that the apparent decline in rates over time is caused by mutational saturation. Using a rate curve estimated from the d-loop data, several dates for last common ancestors were calculated: modern humans and Neandertals (354 ka; 222-705 ka), Neandertals (108 ka; 70-156 ka), and modern humans (76 ka; 47-110 ka). If the rate curve for a particular taxonomic group can be accurately estimated, it can be a useful tool for correcting divergence date estimates by taking the rate decay into account. Our results show that it is invalid to extrapolate molecular rates of change across different evolutionary timescales, which has important consequences for studies of populations, domestication, conservation genetics, and human evolution.

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Is a new and general theory of molecular systematics emerging?

Scott Edwards (2009)

The advent and maturation of algorithms for estimating species trees-phylogenetic trees that allow gene tree heterogeneity and whose tips represent lineages, populations and species, as opposed to genes-represent an exciting confluence of phylogenetics, phylogeography, and population genetics, and ushers in a new generation of concepts and challenges for the molecular systematist. In this essay I argue that to better deal with the large multilocus datasets brought on by phylogenomics, and to better align the fields of phylogeography and phylogenetics, we should embrace the primacy of species trees, not only as a new and useful practical tool for systematics, but also as a long-standing conceptual goal of systematics that, largely due to the lack of appropriate computational tools, has been eclipsed in the past few decades. I suggest that phylogenies as gene trees are a "local optimum" for systematics, and review recent advances that will bring us to the broader optimum inherent in species trees. In addition to adopting new methods of phylogenetic analysis (and ideally reserving the term "phylogeny" for species trees rather than gene trees), the new paradigm suggests shifts in a number of practices, such as sampling data to maximize not only the number of accumulated sites but also the number of independently segregating genes; routinely using coalescent or other models in computer simulations to allow gene tree heterogeneity; and understanding better the role of concatenation in influencing topologies and confidence in phylogenies. By building on the foundation laid by concepts of gene trees and coalescent theory, and by taking cues from recent trends in multilocus phylogeography, molecular systematics stands to be enriched. Many of the challenges and lessons learned for estimating gene trees will carry over to the challenge of estimating species trees, although adopting the species tree paradigm will clarify many issues (such as the nature of polytomies and the star tree paradox), raise conceptually new challenges, or provide new answers to old questions.

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Author and article information

Journal

Journal ID (nlm-ta): BMC Evol Biol

Journal ID (iso-abbrev): BMC Evol. Biol

Title: BMC Evolutionary Biology

Publisher: BioMed Central

ISSN (Electronic): 1471-2148

Publication date Collection: 2013

Publication date (Electronic): 4 September 2013

Volume: 13

Page: 183

Affiliations

[1 ]Key Laboratory of Zoological Systematics and Evolution, Institute of Zoology, Chinese Academy of Sciences, Beijing 100101, China

[2 ]University of Chinese Academy of Sciences, Beijing 100049, China

Article

Publisher ID: 1471-2148-13-183

DOI: 10.1186/1471-2148-13-183

PMC ID: 3766682

PubMed ID: 24006950

SO-VID: 9a4e72bc-a4e8-44a6-99c4-9303e84a4b96

License:

This is an Open Access article distributed under the terms of the Creative Commons Attribution License ( http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Ancient lineage, young troglobites: recent colonization of caves by Nesticella spiders

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Evolutionary Cell Biology

Most cited references 35

Bayesian species delimitation using multilocus sequence data.

Time dependency of molecular rate estimates and systematic overestimation of recent divergence times.

Is a new and general theory of molecular systematics emerging?

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