Development as an Evolutionary Process in Astyanax Cavefish

Jeffery, William R.; Strickler, Allen

doi:10.1201/ebk1578086702-c6

Cited by 6 publications

(15 citation statements)

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“…In cave-dwelling Astyanax and Rhamdia , early eye development already starts with a smaller eye primordium, and culminates in subsequent eye growth arrest [41], [42], [68]. Even though cave molly adults have reduced eye size compared to surface and sulphur mollies, this reduction in eye size appears to be mainly the product of growth arrest during the later developmental stages (stage 35 – stage 50) rather than resulting from disproportionally smaller eye primordia at stage 10.…”

Section: Discussionmentioning

confidence: 99%

Shared and Unique Patterns of Embryo Development in Extremophile Poeciliids

et al. 2011

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BackgroundClosely related lineages of livebearing fishes have independently adapted to two extreme environmental factors: toxic hydrogen sulphide (H2S) and perpetual darkness. Previous work has demonstrated in adult specimens that fish from these extreme habitats convergently evolved drastically increased head and offspring size, while cave fish are further characterized by reduced pigmentation and eye size. Here, we traced the development of these (and other) divergent traits in embryos of Poecilia mexicana from benign surface habitats (“surface mollies”) and a sulphidic cave (“cave mollies”), as well as in embryos of the sister taxon, Poecilia sulphuraria from a sulphidic surface spring (“sulphur mollies”). We asked at which points during development changes in the timing of the involved processes (i.e., heterochrony) would be detectible.Methods and ResultsData were extracted from digital photographs taken of representative embryos for each stage of development and each type of molly. Embryo mass decreased in convergent fashion, but we found patterns of embryonic fat content and ovum/embryo diameter to be divergent among all three types of mollies. The intensity of yellow colouration of the yolk (a proxy for carotenoid content) was significantly lower in cave mollies throughout development. Moreover, while relative head size decreased through development in surface mollies, it increased in both types of extremophile mollies, and eye growth was arrested in mid-stage embryos of cave mollies but not in surface or sulphur mollies.ConclusionOur results clearly demonstrate that even among sister taxa convergence in phenotypic traits is not always achieved by the same processes during embryo development. Furthermore, teleost development is crucially dependent on sufficient carotenoid stores in the yolk, and so we discuss how the apparent ability of cave mollies to overcome this carotenoid-dependency may represent another potential mechanism explaining the lack of gene flow between surface and cave mollies.

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Section: Discussionmentioning

confidence: 99%

Shared and Unique Patterns of Embryo Development in Extremophile Poeciliids

et al. 2011

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“…That troglomorphic species can evolve in such relatively environmentally benign environments (except for the absence of light) is given credence by the recent work of Jeffery and his colleagues (Jeffery, ; Jeffery & Strickler, ; Bilandžija et al ., ). Caves with Astyanax have abundant food, at least compared to most caves, and have both daily (bat movements) and seasonal (flooding) environmental cycles.…”

Section: Making Sense Of Troglomorphymentioning

confidence: 91%

“…Convergence has been reinforced in a phylogenetic context by Hedin and colleagues (Hedin & Thomas, ; Derkarabetian, Steinmann & Hedin, ) studying harvestmen, where they found ‘repeated and time‐correlated morphological convergence.’ Among cave‐ and spring‐dwelling populations of the amphipod Gammarus minus Say, Culver, Kane & Fong () found that selection intensity on eye size was in the opposite direction in the two habitats (favouring large eyes in springs and small eyes in caves), as expected under the neo‐Darwinian paradigm. Finally, Jeffery and colleagues (Jeffery, ; Yamamoto et al ., ; Jeffery & Strickler, ) demonstrated pleiotropic effects of genes involved in eye development in the cave fish Astyanax mexicanus (De Filippi), implying that strong natural selection is involved in eye loss in caves. This work also appears to resolve the controversy between selection and neutral mutation (Culver & Wilkens, ) largely in favour of natural selection (but see also Wilkens, ), although neutral mutation may still have a role in the number of melanophore cells produced during development in cave animals (Protas et al ., ).…”

Section: Introductionmentioning

confidence: 99%

Convergence and divergence in the subterranean realm: a reassessment

Pipan

Culver

2012

Biological Journal of the Linnean Society

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The dominant neo-Darwinian paradigm of the evolution of cave animals is that the severe aphotic, low food environment with little environmental cyclicity imposes strong selective pressures leading to a convergent (troglomorphic) morphology of reduced pigment and eyes, and elaborated extra-optic sensory structures. Challenges to the paradigm come from two fronts. First, troglomorphic animals occur in many aphotic habitats with relatively abundant food and environmental cyclicity. Second, many permanent reproducing populations in caves are not troglomorphic. A review of data on patterns of troglomorphy confirms both of these points. This suggests that the absence of light, rather than resource level and environmental cyclicity, is the important selective factor, and that other forces are at work, including competition and differences in the age of lineages in subterranean environments.

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“…These studies show that only few and homologous genes are involved in the eye reduction of vertebrates [4] and crustaceans [23,24]. More importantly, in A. mexicanus mutations only affect lens apoptosis, whereas all other rsbl.royalsocietypublishing.org Biol Lett 9: 20121098 genes involved in eye development seem to stay intact [4], which would be unlikely in the case of relaxed selection. Also, some genes involved in eye development (like sonic hedgehog) have an increased expression, and are not simply shut down [4].…”

Section: Discussionmentioning

confidence: 89%

“…More importantly, in A. mexicanus mutations only affect lens apoptosis, whereas all other rsbl.royalsocietypublishing.org Biol Lett 9: 20121098 genes involved in eye development seem to stay intact [4], which would be unlikely in the case of relaxed selection. Also, some genes involved in eye development (like sonic hedgehog) have an increased expression, and are not simply shut down [4]. In contrast to eye reduction, loss of pigmentation in Astyanax was proposed to be caused by neutral mutations, as the involved genes are both upand downregulated, and thus not driven in one direction rsbl.royalsocietypublishing.org Biol Lett 9: 20121098 via selection [13].…”

Section: Discussionmentioning

confidence: 99%

Rapid evolution of troglomorphic characters suggests selection rather than neutral mutation as a driver of eye reduction in cave crabs

et al. 2013

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This study asked whether reductive traits in cave organisms evolve at a slower pace (suggesting neutral evolution under relaxed selection) than constructive changes, which are likely to evolve under directional selection. We investigated 11 subterranean and seven surface populations of Sundathelphusa freshwater crabs on Bohol Island, Philippines, and examined constructive traits associated with improved food finding in darkness (increased leg and setae length) and reductive traits (reduced cornea size and eyestalk length). All changes occurred rapidly, given that the age of the most recent common ancestor was estimated to be 722-271 ka based on three mitochondrial markers. In order to quantify the speed of character change, we correlated the degree of morphological change with genetic distances between surface and subterranean individuals. The temporal pattern of character change following the transition to subterranean life was indistinguishable for constructive and reductive traits, characterized by an immediate onset and rapid evolutionary change. We propose that the evolution of these reductive traits-just like constructive traits-is most likely driven by strong directional selection.

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Development as an Evolutionary Process in Astyanax Cavefish

Cited by 6 publications

References 0 publications

Shared and Unique Patterns of Embryo Development in Extremophile Poeciliids

Shared and Unique Patterns of Embryo Development in Extremophile Poeciliids

Convergence and divergence in the subterranean realm: a reassessment

Rapid evolution of troglomorphic characters suggests selection rather than neutral mutation as a driver of eye reduction in cave crabs

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