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.