Cave Evolution

Abstract

Cave‐dwelling animals are fascinating because of the phenotypic extremes they frequently exhibit, such as a reduced or complete loss of 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 often attributed to the paucity of 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‐dwelling and intra‐specific ‘surface’ forms reveal numerous morphological changes associated with cave adaptation are recessive.

  • Phenotypic analyses in subsequent generations reveal many cave‐associated characteristics arise through Mendelian (single locus) and complex (polygenic) patterns of inheritance.

  • The cave environment likely represents 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.

Keywords: troglomorphy; troglobites; troglophiles; karst; evolution and development; QTL analysis

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).

close

References

Ashmole NP and Ashmole MJ (2000) Fallout of dispersing arthropods supporting invertebrate communities in barren volcanic habitats. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 269–286. Amsterdam: Elsevier.

Avise JC and Selander RK (1972) Evolutionary genetics of cave‐dwelling fishes of the genus Astyanax. Evolution 26: 1–19.

Barr TC (1968) Cave ecology and the evolution of troglobites. Evolutionary Biology 2: 35–102.

Borowsky R (2008) Restoring sight in blind cavefish. Current Biology 18: R23–R24.

Burbanck WD, Edwards JP and Burbanck MP (1948) Toleration of lowered oxygen tension in cave and stream crayfish. Ecology 29: 360–367.

Cavallari N, Frigato E, Vallone D et al. (2011) A blind circadian clock in cavefish reveals that opsins mediate peripheral clock photoreception. PLoS Biology 9: e1001142.

Culver DC, Kane TC and Fong DW (1995) Adaptation and natural selection in caves: the evolution of Gammarus minus. Cambridge, MA: Harvard University Press, 223 pp.

Culver DC (1982) Cave Life: Evolution and Ecology. Cambridge, MA: Harvard University Press, 189 pp.

Culver DC and Holsinger JR (1992) How many species of troglobites are there? National Speleological Society Bulletin 54: 79–80.

Culver DC and Poulson TL (1971) Oxygen consumption and activity in closely related amphipod populations from cave and surface habitats. American Midland Naturalist 85: 74–84.

Culver DC and Wilkens H (2000) Critical review of the relevant theories of the evolution of subterranean animals. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 381–398. Amsterdam: Elsevier.

Darwin C (1859) On the Origin of Species by Means of Natural Selection, or the Preservation of Favoured Races in the Struggle for Life. London, UK: John Murray.

Deharveng L and Bedos A (2000) The cave fauna of Southeast Asia. Origin, evolution and ecology. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 603–632. Amsterdam: Elsevier.

Dickson GW, Patton JC, Holsinger JR and Avise JC (1979) Genetic variation in cave‐dwelling and deep‐sea organisms, with emphasis on Crangonyx antennatus (crustacea: Amphipoda) in Virginia. Brimleyana 2: 119–130.

Elliott WR (2000) Conservation of the North American cave and karst biota. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 665–689. Amsterdam: Elsevier.

Gnaspini P and Trajano E (2000) Guano communities in tropical caves. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 251–268. Amsterdam: Elsevier.

Gross JB, Borowsky R and Tabin CJ (2009) A novel role for Mc1r in the parallel evolution of depigmentation in independent populations of the cavefish Astyanax mexicanus. PLoS Genetics 5(1): e1000326.

Hamilton‐Smith E and Eberhard S (2000) Conservation and cave communities in Australia. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 647–664. Amsterdam: Elsevier.

Harvey MS, Shear WA and Hoch H (2000) Onychophora, Arachnida, Myriapods and Insecta. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 79–94. Amsterdam: Elsevier.

Hobbs HH (2000) Crustacea. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 95–107. Amsterdam: Elsevier.

Hoch H (2000) Acoustic communication in darkness. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 211–220. Amsterdam: Elsevier.

Holsinger JR (2000) Ecological derivation, colonization, and speciation. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 399–415. Amsterdam: Elsevier.

Hüppop K (2000) How do cave animals cope with the food scarcity in caves? In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 159–188. Amsterdam: Elsevier.

Iliffe TM (2000) Anchialine cave ecology. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 59–76. Amsterdam: Elsevier.

Jasinska EJ and Knott B (2000) Root‐driven faunas in cave waters. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 287–307. Amsterdam: Elsevier.

Juberthie C (1969) Relations entre le climat, le microclimat et les Aphaenops cerberus dans lagrotte de Sainte‐Catherine (Ariege). Annales deSpeélélogie 24: 75–104.

Juberthie C (2000a) Conservation of subterranean habitats and species. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 691–700. Amsterdam: Elsevier.

Juberthie C (2000b) The diversity of the karstic and pseudokarstic hypogean habitats in the world. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 17–39. Amsterdam: Elsevier.

Kane TC and Poulson TL (1976) Foraging by cave beetles: spatial and temporal heterogeneity of prey. Ecology 57: 793–800.

Kosswig C (1948) Genetische beiträge zur praadaptations‐theorie. Revue de Facultie des Science (Istanbul) Series B 5: 176–209.

Kosswig C (1965) Génétique et évolution régressive. Revue des Questions Scientifiques 136: 227–257.

Kosswig C and Kosswig L (1940) Die variabilität bei asellus aquaticus unter besonderer berucksichtigung der variabilität in isolierten unter‐und aberirdischen population. Revue de Facultie des Science (Istanbul) Series B 5: 1–55.

Langecker TG (2000) The effects of continuous darkness on cave ecology and caverniculous evolution. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 135–157. Amsterdam: Elsevier.

Maguire B (1961) Regressive evolution in cave animals and its mechanism. Texas Journal of Science 13: 363–370.

Mitchell RW, Russell WH and Elliott WR (1977) Mexican Eyeless Characin Fishes, Genus Astyanax: Environment, Distribution, and Evolution. Lubbock, TX: Texas Tech Press.

Nevo E (1976) Adaptive strategies of genetic systems in constant and varying environments. In: Karlin S and Nevo E (eds) Population Genetics and Ecology, pp. 141–158. New York: Academic Press.

Ornelas‐García CP, Dominguez‐Dominguez O and Doadrio I (2008) Evolutionary history of the fish genus Astyanax Baird & Girard (1854) (Actinopterygii, Characidae) in Mesoamerica reveals multiple morphological homoplasies. BMC Evolutionary Biology 8: 340.

Parzefall J (2000) Ecological role of aggressiveness in the dark. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 221–228. Amsterdam: Elsevier.

Pottin K, Hyacinthe C and Retaux S (2010) Conservation, development, and function of a cement gland‐like structure in the fish Astyanax mexicanus. Proceedings of the National Academy of Sciences of the USA 107: 17256–17261.

Poulson TL (1963) Cave adaptation in amblyopsid fishes. American Midland Naturalist 70: 257–290.

Poulson TL (1981) Variations in life history of linyphiid cave spiders. Proceedings of the Eighth International Congress of Speleology, Bowling Green, Kentucky 1: 60–62.

Poulson TL and Lavoie KH (2000) The trophic basis of subsurface ecosystems. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 231–249. Amsterdam: Elsevier.

Protas ME, Hersey C, Kochanek D et al. (2006) Genetic analysis of cavefish reveals molecular convergence in the evolution of albinism. Nature Genetics 38: 107–111.

Protas ME, Trontelj P and Patel NH (2011) Genetic basis of eye and pigment loss in the cave crustacean, Asellus aquaticus. Proceedings of the National Academy of Sciences of the USA 108: 5702–5707.

Racovitza EG (1907) Essai sur les problémes biospéologiques. Archives de Zoologie Expérimentale et Générale 6: 371–488.

Sadoglu P (1979) A breeding method for blind Astyanax mexicanus based on annual spawning patterns. Copeia 1979: 369–371.

Sarbu SM (2000) Movile cave: a chemoautotrophically based groundwater ecosystem. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 319–343. Amsterdam: Elsevier.

Sbordoni V, Allegrucci G and Cesaroni D (2000) Population genetic structure, speciation, and evolutionary rates in cave‐dwelling organisms. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems, pp. 453–477. Amsterdam: Elsevier.

Schlagel SR and Breder CM (1947) A study of oxygen consumption of blind and eyed cave characins in light and in darkness. Zoologica 32: 17–28.

Selander RK (1976) Genic variation in natural populations. In: Ayala J (ed.) Molecular Evolution, pp. 21–45. Sunderland, MA: Sinauer Associates.

Weber A (2000) Fish and amphibia. In: Wilkens H, Culver DC and Humphreys WF (eds) Subterranean Ecosystems pp. 109–132. Amsterdam: Elsevier.

Wilkens H (1971) Genetic interpretation of regressive evolutionary processes: studies on hybrid eyes of two Astyanax populations (characidae, pisces). Evolution 25: 530–544.

Wilkens H (1988) Evolution and genetics of epigean and cave Astyanax fasciatus (Characidae, Pisces): support for the neutral mutation theory. In: Hecht MK and Wallace B (eds) Evolutionary Biology, pp. 271–367. New York, NY: Plenum Publishing Corporation.

Wright S (1964) Pleiotropy in the evolution of structural reduction and of dominance. American Naturalist 98: 65–70.

Yamamoto Y, Byerly MS, Jackman WR and Jeffery WR (2009) Pleiotropic functions of embryonic sonic hedgehog expression link jaw and taste bud amplification with eye loss during cavefish evolution. Developmental Biology 330: 200–211.

Yoshizawa M, Goricki S, Soares D and Jeffery WR (2010) Evolution of a behavioral shift mediated by superficial neuromasts helps cavefish find food in darkness. Current Biology 20: 1631–1636.

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.

Eigenmann CH (1909) Cave Vertebrates of America: A Study in Degenerative Evolution. Washington, DC, USA: The Carnegie Institution of Washington.

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 USA 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.

Wilkens H and Strecker U (2003) Convergent evolution of the cavefish Astyanax (Characidae: Teleostei): genetic evidence from reduced eye‐size and pigmentation. Biological Journal of the Linnean Society 80: 545–554.

Wilkens H (2010) Genes, modules and the evolution of cave fish. Heredity 105: 413–422.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Gross, Joshua B(Jan 2012) Cave Evolution. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0023628]