Cave Evolution

Abstract

Cave‐dwelling animals are fascinating because of the phenotypic extremes they frequently exhibit, such as a reduced vision and pigmentation. Equally interesting is the fact that irrespective of taxonomic position, organisms colonising the subterranean environment converge on highly similar phenotypic deficits and improvements. Thus, a predictable suite of morphological, physiological and behavioural changes evolve in response to low nutrient conditions of the subterranean environment. Despite several decades of enquiry, the precise genetic and molecular underpinnings of cave‐associated changes are only beginning to be elucidated through the use of high‐resolution contemporary molecular and genetic techniques. Regressive phenotypic changes, those traits that are lost in derived lineages, are particularly interesting since they evolve in the absence of obvious selective value to the organism. Continuing research utilising an increasing number of emerging cave‐dwelling models offers the exciting prospect of clarifying longstanding problems in contemporary evolutionary biology.

Key Concepts

  • Widespread convergence on cave‐associated (troglomorphic) characteristics is frequently attributed to the reduced nutrition and overall stability of the cave environment.
  • Cave‐adapted organisms are excellent models for the study of regressive phenotypic evolution, that is. the loss of traits in derived organisms.
  • The evolutionary mechanism(s) accounting for phenotypic loss in cave‐dwelling organisms (neutralism versus selection) remains unknown.
  • Hybrid crosses between cave‐ and surface‐dwelling morphs demonstrate that numerous morphological changes associated with cave adaptation are recessive.
  • Phenotypic analyses in experimental pedigrees have revealed that cave‐associated characteristics arise through both Mendelian (single locus) and complex (polygenic) patterns of inheritance.
  • The cave environment is an attractive habitat given that over 50 000 cave‐limited species are known worldwide, distributed across broad taxonomic groups.
  • Contemporary cave research has advanced significantly over the last decade thanks to integrative analyses combining developmental, genetic, genomic, behavioural, physiological and population‐level approaches.
  • Genomic and transcriptomic techniques are providing new insights to the underlying genetic changes mediating cave evolution, and how genomes evolve in the subterranean habitat.

Keywords: regressive trait evolution; subterranean; troglomorphy; karst; constructive trait evolution; preadaptation

Figure 1. Degree of troglomorphy as an estimate of time since isolation in the cave environment. Several authors have argued that more extreme cave‐associated characters reflect a longer period of isolation from surface‐dwelling ancestors. Accordingly, the length of time an organism has been confined to the cavernous environment (x‐axis) is directly associated with their of extent cave‐associated phenotypes (y‐axis). This is a reasonable metric; however, it assumes that the principal mechanism driving the evolution of regressive characters is neutral mutation. As such, it does not account for the possibility that cave‐associated traits may evolve rapidly under strong selective forces (A*). Alternatively, this metric does not account for the scenario in which an ancient cave population retains surface‐like characteristics (B*). This could arise through introgressive hybridisation with local surface forms, as has been reported for Astyanax.
Figure 2. Widespread convergence on troglomorphic characteristics is evident from distant taxonomic groups. Irrespective of phylogenetic position, organisms that colonise the cave environment undergo similar phenotypic changes. Examples of emerging model systems include the teleost fish (Astyanax mexicanus) from NE Mexico and isopods (Asellus aquaticus) from the karst region of southern Slovenia (a). In both instances, an extant surface‐dwelling counterpart still resides in the overlying environment. These surface forms retain the ability to produce viable offspring when hybridised with the cave morphotype, enabling advanced genetic analysis. Having colonised the cave environment, subterranean forms no longer experience sunlight (b), and evolve a series of regressive (red arrow, box) and constructive (green arrow, box) changes that facilitate success in complete darkness (c).
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Further Reading

Borowsky R and Wilkens H (2002) Mapping a cave fish genome: polygenic systems and regressive evolution. Journal of Heredity 93: 19–21.

Dowling TE, Martasian DP and Jeffery WR (2002) Evidence for multiple genetic forms with similar eyeless phenotypes in the blind cavefish, Astyanax mexicanus. Molecular Biology and Evolution 19: 446–455.

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Gross JB, Protas M, Conrad M, et al. (2008) Synteny and candidate gene prediction using an anchored linkage map of Astyanax mexicanus. Proceedings of the National Academy of Sciences of the United States of America 105: 20106–20111.

Jeffery WR (2008) Emerging model systems in evo‐devo: cavefish and microevolution of development. Evolution & Development 10: 265–272.

Jeffery WR (2010) Pleiotropy and eye degeneration in cavefish. Heredity 105: 495–496.

Panaram K and Borowsky R (2005) Gene flow and genetic variability in cave and surface populations of the Mexican tetra, Astyanax mexicanus (Teleostei: Characidae). Copeia 2005: 409–416.

Protas M, Tabansky I, Conrad M, et al. (2008) Multi‐trait evolution in a cave fish, Astyanax mexicanus. Evolution & Development 10: 196–209.

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Gross, Joshua B, and Berning, Daniel J(Dec 2018) Cave Evolution. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023628.pub2]