Thesis

The evolutionary ecology of the cave molly (Poecilia mexicana) from the Cueva del Azufre system effects of abiotic and biotic environmental conditions

Tobler, M

Record Number:
2342
Year:
2008
Pages:
150 pages
University:
University of Zurich
Abstract:
Caves, with their divergent environmental conditions, provide some of the most unusual habitats on earth and harbor a diversity of highly adapted endemic organisms. Many aspects of the ecology and evolution of cave organisms, however, are poorly understood; probably because the inaccessibility of their habitats, the often small population sizes and their conservation status, as well as the lack of closely related epigean species that would allow for comparative studies. For my thesis, I explore how divergent abiotic conditions and correlated biotic conditions affect the ecology of a small livebearing fish occurring in cave as well as in surface habitats. Furthermore, I identify the evolutionary responses to selective pressures imposed by the environment, ultimately with the goal to contribute to the understanding of the processes that lead to ecological and phenotypic diversity and speciation. Chapter 1 provides a short introduction to pertinent concepts in cave biology and a synthesis of my major research questions and results. My research was conducted in Cueva del Azufre system in southern Mexico where the study species (Poecilia mexicana, Poeciliidae) has occurs in four habitat types: non-sulfidic surface, sulfidic surface, non-sulfidic cave, and sulfidic cave. Chapters 2 & 3 provide an introduction and characterization the abiotic and biotic environmental factors in the study system. Specifically, the distribution of toxic hydrogen sulfide (H2S) is investigated in chapter 2, and a newly discovered cave population of P. mexicana is described in chapter 3. The Cueva del Azufre system provides an unparalleled ‘natural experiment’ with two strong selective pressures (the presence or absence of light and H2S) occurring in a fully 2x2 factorial design. For chapter 4, I investigated the genetic and phenotypic differentiation of P. mexicana in different habitat types using molecular genetic and morphological analyses. I document independent and partially heritable morphological variation along each environmental gradient. Molecular genetic analyses using microsatellites as well as cytochrome b gene sequences indicate high population differentiation and very low rates of gene flow among populations from different habitat types despite the spatial proximity and the lack of physical barriers. Altogether, the study provides evidence for parapatric adaptive divergence in response to divergent natural selection by abiotic environmental conditions. For chapter 5, I investigated differences in the tropic ecology of P. mexicana in the different habitat types. Resource use in different habitat types was investigated using gut content analysis. A shift in resource use, from algivory/ detrivory to the incorporation of invertebrate food items, was detected upon colonization of the divergent habitats. P. mexicana in cave habitats further exhibited a higher dietary niche width than conspecifics from surface habitats. Condition of P. mexicana was analyzed using storage lipid extractions, and fish from sulfidic and cave habitats exhibited a very poor condition hinting towards resource limitation or high costs of coping with extreme conditions. Finally, the shift in resource use was accompanied by divergence in viscerocranial morphology. Although the divergent morphological traits investigated were phenotypically plastic to some extent, they appear to have a genetic basis. It is suggested that the morphological diversification is an adaptation to the differential use of resources among populations. Caves are often assumed to be predator-free environment for cave fishes. This has been proposed to be a potential benefit of colonizing these otherwise relatively hostile environments. In chapters 6, I tested this hypothesis by investigating the predator-prey interaction of a belostomatid water-bug (predator) and P. mexicana. I determined feeding rates and size-specific prey preferences of the predator, and estimated the population density of Belostoma using a mark-recapture analysis. Belostomatids were found to heavily prey on cave mollies and to exhibit a prey preference for large bodied fish. The mark-recapture analysis revealed a high population density of the heteropterans in the cave. Although the absence of predators is not a general habitat feature of cavernicolous P. mexicana, this study highlights the fundamental differences in predatory regimes between epigean and cave habitats. In chapter 7, I suggest that extreme environments in general, and cave habitats in particular, may function as refuge from parasite infections, since parasites can become locally extinct either directly, through selection by an extreme environmental parameter on free-living parasite stages, or indirectly, through selection on other host species involved in its life cycle. Populations from such sulfidic and cave habitats are significantly less parasitized by the trematode Uvulifer sp. than populations from a non-sulfidic habitat and it is suggested that reduced parasite prevalence may be a benefit of colonizing otherwise inhospitable habitats. Finally, in chapter 8, I provide some conclusion of my thesis and perspectives for future research.
Times Cited:
1
Related Records:
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A review of morphological and behavoural changes in the cave molly, Poecilia mexicana, from Tabasco, Mexcio
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Sex recognition and female preferences of cave mollies Poecilia mexicana during the sexual cycle
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Sex recognition and female preferences of cave mollies poecilia mexicana in light and darkness
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Troglomorphy in the cave fish Poecilia mexicana from Cueva de Villa Luz, Tabasco, Mexico
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Biodiversity of terrestrial microarthropods from Las Sardinas Cave, Tabasco, Mexico
Plath, M, Korner, KE, Parzefall, J and Schlupp, I (2003)
Persistence of a visually mediated mating preference in the cave molly, Poecilia mexicana (Poeciliidae, Teleostei)
Plath, M, Parzefall, J and Schlupp, I (2003)
The role of sexual harassment in cave and surface dwelling populations of the Atlantic molly, Poecilia mexicana (Poeciliidae, Teleostei)
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Sex recognition in in surface and cave dwelling male Atlantic mollies, Poecilia mexicana (Poeciliidae, Teleostei)
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Shoaling behaviour in a surface-dwelling and cave-dwelling population of a barb Garra barreimiae (Cyprinidae: Teleostei)
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Does sexual experience influence mate choice descisions in cave molly females (Poecilia mexicana, Poeciliidae, Teleostei)?
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Size-dependent male mating behaviour in the cave molly, Poecilia mexicana (Poeciliidae, Teleostei)
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Sexual harassment in a live-bearing fish (Poecilia mexicana): influence of population-specific male mating behaviour
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Sexual selection in darkness: female mating preferences in surface and cave dwelling Atlantic mollies, Poecilia mexicana (Poeciliidae, Teleostei)
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Cave molly males (Poecilia mexicana) do not recognise receptive females without body contact
Plath, M, Tobler, M and Schlupp, I (2004)
Cave fish looking for mates: A visual mating preference in surface and cave-dwelling Atlantic mollies (Poecilia mexicana, oeciliidae)
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Imperfect signal transmission and female mate choice in surface- and cave-dwelling Atlantic mollies, Poecilia mexicana (Poeciliidae, Teleostei)
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Cave molly females (Poecilia mexicana, Poeciliidae, Teleostei) like well-fed males
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Field observations on male mating behaviour in surface and cave-dwelling Atlantic mollies (Poecilia mexicana, Poeciliidae)
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Non-visual localisation of a conspecific male by surface and cave-dwelling Atlantic molly females (Poecilia mexicana, Poeciliidae, Teleostei)
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Homosexual behaviour in a cavernicolous fish, Poecilia mexicana (Poeciliidae, Teleostei)
Riesch, R, Schlupp, I, Tobler, M, Garcia de Leon, FJ and Plath, M (2006)
Reduction of the association preference for conspecifics in cave-dwelling Atlantic mollies, Poecilia mexicana
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Variability in troglomorphic adaptations of a mexican cavefish, Poecilia mexicana, from Tabasco, Mexico
Plath, M, Tobler, M, Riesch, R, Garcia de Leon, FJ and Schlupp, I (2006)
Evolutionary biology and Cueva de Villa Luz: Ichthyological research in a sulfidic cave in Tabasco
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Reduction of a visually mediated association preference in the cave molly (Poecilia mexicana, Poeciliidea, Teleostei)
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Choosy males from underground: male mating preferences in surface- and cave-dwellind Atlantic mollies (Poecilia mexicana)
Riesch, R, Schlupp, I and Plath, M (2006)
Influence of male competition on male mating behaviour in the cave molly, Poecilia mexicana
Plath, M, Schlupp, I, Parzefall, J and Riesch, R (2007)
Female choice for large body size in the cave molly Poecilia mexicana (Poeciliidae, Teleostei): influence od species- and sex-specific cues
Tobler, M, Schlupp, I and Plath, M (2007)
Predation of a cave fish (Poecilia mexicana, Poeciliidae) by a giant water bug (Belostoma, Belostomatidae) in a Mexican sulphur cave
Plath, M., Hauswaldt, J.S., Moll, K., Tobler, M., Garcia de Leon, F.J., Schlupp, I. and Tiedemann, R. (2007)
Local adaptation and pronounced genetic differentiation in an extremophile fish, Poecilia mexicana, inhabiting a Mexican cave with toxic hydrogen sulfide
Plath, M. and Tobler, M. (2007)
Sex recognition in surface- and cave-dwelling Atlantic molly females (Poecilia mexicana, Poeciliidae, Teleostei): influence of visual and non-visual cues
Plath, M and Schlupp, I (2008)
Parallel evolution leads to reduced shoaling behaviour in two cave dwelling populations of Atlantic mollies (Poecilia mexicana, Poeciliidae, Teleostei)
Tobler, M, Riesch, R, Garcia de Leon, FJ, Schlupp, I and Plath, M (2008)
A new and morphologically distinct population of cavernicolous Poecilia mexicana (Poeciliidae: Teleostei)
Tobler, M, DeWhitt, TJ, Schlupp, I, Garcia de Leon, FJ, Herrmann, R, Feulner, PGD, Tiedemann, R and Plath, M (2008)
Toxic hydrogen sulfide and dark caves: Phenotypic and genetic divergence across two abiotic environmental gradients in Poecilia mexicana
Parzefall, J and Plath, M (2008)
Evolutionary ecology of the Mexican cavefish Poecilia mexicana (Poeciliidae) compared to epigean relatives
Plath, M (2008)
Male mating behaviour and costs of sexual harassment for females in cavernicolous and extremophile populations of Atlantic mollies (Poecilia mexicana)
Tobler, M (2008)
The evolutionary ecology of the cave molly (Poecilia mexicana) from the Cueva del Azufre system effects of abiotic and biotic environmental conditions
Timmermann, M and Plath, M (2009)
Phototactic response and light sensitivity in an epigean and a hypogean population of a barb (Garra barreimiae, Cyprinidae)
Riesch, R, Duwe, V, Hermann, N, Padur, L, Ramm, A, Scharnweber, K, Schulte, M, Schulz-Mirbach, T, Ziege, M and Plath, M (2009)
Variation along the shy-bold continuum in extremophile fishes (Poecilia mexicana, P. sulphuraria)
Riesch, R, Tobler, M, Plath, M and Schlupp, I (2009)
Offspring number in a livebearing fish (Poecilia mexicana: Poeciliidae): reduced fecundity and reduced plasticity in a population of cave mollies
Riesch, R, Plath, M and Schlupp, I (2010)
Toxic Hygrogen sulphide and dark caves: life history adaptations to extreme environments in a livebearing fish (Poecilia mexicana, Poeciliidae)
Plath, M, Richter, S, Schlupp, I and Tiedemann, R (2010)
Misleading mollies: Surface but not cave dwelling Poecilia mexicana males deceive competitors about mating preferences
Plath, M and Tobler, M (2010)
Subterranean fishes of Mexico (Poecilia mexicana, Poeciliidae)
Schulz-Mirbach, T, Ladich, F and Riesch, R (2010)
Otolith morphology and hearing abilities in cave- and surface-dwelling ecotypes of the Atlantic molly, Poecilia mexicana (Teleostei: Poeciliidae).
Roach, KA, M, Tobler and Winemiller, KO (2011)
Hydrogen sulfide, bacteria and fish: a unique subterranean food chain
Tobler, M and Plath, M (2011)
Living in extreme environments
Riesch, R, Plath, M and Schlupp, I (2011)
Toxic hydrogen sulphide and dark caves: pronounced male life-history divergance among locally adapted Poecilia mexicana ((Poeciliidae)
Palacios-Vargas, J.G., Castano-Meneses, G. and Estrada, D.A. (2011)
Diversity and dynamics of microarthropods from different biotopes of Las Sardinas cave (Mexico)
Plath, M, Riesch, R, Culumber, Z, Streit, B and Tobler, M (2011)
Giant water bug (Belostoma sp.) predation on a cave fish (Poecilia mexicana): effects of female body size and gestational state
R, Riesch, I, Schlupp, Schleucher, Elke, Hildenbrand, Phillipp, Kohler, A, Arias Rodriguez, Lenin and Plath, M (2011)
Reduced starvation resistance and increased metabolic rates in an unusual cave organism: the cave molly (Poecilia mexicana: Poeciliidae)
Mejia, R (2011)
Cave-dwelling fish provide clues to the circadian cycle
Kelley, J.L., Passow, C.N., Plath, M., Rodriguez, L.A., Yee, M.C. and Tobler,M. (2012)
Genomic resources for a model in adaptation and speciation research: characterization of the Poecilia mexicana transcriptome
Tobler, M., Roach, K., Winemiller, K.O., Morehouse, R.L. and Plath M. (2013)
Population Structure, Habitat Use, and Diet of Giant Waterbugs in a Sulfidic Cave
Rosales Lagarde, L (2013)
Sulfidic karst springs and speleogenesis in the Sierra de Chiapas
Schlupp, I., Colston, T. J., Joachim, B. L. and Riesch, R. (2013)
Translocation of cave fish (Poecilia mexicana) within and between natural habitats along a toxicity gradient
Ruschenbaum, S. and Schlupp, I. (2013)
Non-Visual Mate Choice Ability in a Cavefish (Poecilia mexicana) is not mechanosensory
Joachim, B. L., R, Riesch and Jeffery, WR (2013)
Pignent cell retention in cavernicolous populations of Poecilia mexicana (Poeciliidae)
Plath, M, M, Pfenninger, H, Lerp, R, Riesch, Eschenbrenner, C, Slettery, PA, Bierbach, D, N, Herrmann, Schultze, M, Arias Rodriguez, Lenin, JR, Indy, C, Passow and M, Tobler (2013)
Genetic differentiation and selection against migrants in evolutionarily replicated extreme environments
Jourdan J, Bierbach D, Riesch R, Dzienko J, Karau N, Oranth A, Stadler S, Schießl A, Wigh A, Arias-Rodriguez L, Indy JR, Klaus S, Zimmer C and M, Plath (2014)
Microhabitat use, population densities and size distributions of sulfur cave-dwelling Poecilia mexicana
Pfenninger M, Lerp H, Tobler M, Passow C, Kelley JL, Funke E, Greshake B, Erkoc UK, Berberich T and M, Plath (2014)
Parallel evolution of cox-genes in H2S-tolerant fish as key adaptation to a toxic environment
Palacios-Vargas, J.G., Juberthie, C. and Reddell, J. (2014-2015)
Encyclopaedia Biospeologica Mexico
Riesch, R., Tobler, M. and Plath, M. (2015)
Extremophile Fishes: Ecology, Evolution, and Physiology of Teleosts in Extreme Environments
Riesch, R, Tobler, CM and Plath, M (2015)
Hydrogen sulphide-toxic habitats
Plath, M., Tobler, M. and Riesch, R. (2015)
Extremophile fishes: An introduction
Tobler, M. and Riesch, R. and Plath, M. (2015)
Extremophile fishes: An integrative synthesis
Riesch, R., Tobler, C.M., Lerp, H., Jourdan, J., Doumas, T., Nosil, P., Langerhans, R.B. and Plath, M. (2016)
Extremophile Poeciliidae: Multivariate insights into the complexity of speciation along replicated ecological gradients
Palacios, M., Voelker, G. and Rodriguez, L.A. (2016)
Phylogenetic analyses of the subgenus Mollienesia (Poecilis, Poeciliidae, Teleostei) reveal taxonomic inconsistencies, cryptic biodiversity and spatio-temporal aspects of diversification in Middle America
Passow, Courtney N.; Brown, Anthony P.; Arias-Rodriguez, Lenin; et al. (2017)
Complexities of gene expression patterns in natural populations of an extremophile fish (Poecilia mexicana, Poeciliidae)
Passow C.N., Arias-Rodriguez L. and Tobler, M. (2017)
Convergent evolution of reduced energy demands in extremophile fish
Brown, AP, Greenway, R, Morgan, S, Quackenbush, CR, Giordani, L, Arias-Rodriguez, L, Tobler, M and Kelley, JL (2017)
Genome-scale data reveal that endemic Poecilia populations from small sulphidic springs display no evidence of inbreeding
Passow, C.N. (2017)
Organ-specific patterns of gene expression among extremophile fish populations exposed to toxic hydrogen sulfide and permanent darkness
Tobler, M., Kelley, J.L., Plath, M., and Riesch, R. (2018)
Extreme environments and the origins of biodiversity: Adaptation and speciation in sulphide spring fishes
Torres-Dowdall, J., Karagic, N., Plath, M. and Riesch, R. (2018)
Evolution in caves: selection from darkness causes spinal deformities in teleost fishes
Bierbach, D., Lukas. J.A., Bergmann, A., Elsner, K., Höhne, L., Weber, C., Weimar, N., Redriguez, L.A., Mönck, H.J., Nguyen, H., Romanczuk, P., Landgraf, T. and Krause, J. (2018)
Insights into the social behavior of surface and cave-dwelling fish (Poecilia mexicana) in light and darkness through the use of a biomimetic robot
Lau, G.Y., Barts, N., Hartley, R.C., Tobler, M., Richards, J.G., Murphy, M.P. and Arndt, S. (2019)
Detection of changes in mitochondrial hydrogen sulfide in vivo in the fish model Poecilia mexicana (Poeciliidae)
Torres-Martínez, A., Ruiz de Dios, L., Hernández-Franyutti, A., Uribe, M.C., and Sánchez, W.C. (2019)
Structure of the testis and spermatogenesis of the viviparous teleost Poecilia mexicana (Poeciliidae) from an active sulfur spring cave in Southern Mexico