Abstract
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.
Highlights
IntroductionMost studies on ecological speciation in animals have focused on divergent selection as a result of biotic interactions, with populations differing, for example, in resource use [4,5,6,7], predation pressures [8,9], or parasite exposure [10,11,12]
We examined embryos of surface-dwelling P. mexicana from benign surface habitats, cavedwelling P. mexicana from the toxic Cueva del Azufre (‘‘cave mollies’’), and the sulphur-endemic P. sulphuraria from a toxic spring (‘‘sulphur mollies’’) to examine at which points during development the local adaptations in life history and morphology would first be detectable and to what extent convergent phenotypes are the product of convergent developmental modes
We investigated the following four specific questions concerning the development of some key divergent traits in extremophile Poecilia: (1) When and how do cave and sulphur mollies increase offspring size at birth? Extremophile poeciliids could produce larger oocytes, and embryos might take roughly the same developmental route as smaller surface molly embryos
Summary
Most studies on ecological speciation in animals have focused on divergent selection as a result of biotic interactions, with populations differing, for example, in resource use [4,5,6,7], predation pressures [8,9], or parasite exposure [10,11,12]. The concept of stress and maintenance of homeostasis through adaptation to abiotic habitat parameters is often ignored in the study of speciation in animals and more emphasis is put on its role in population decline and extinction [13], even though stressful environments have long been known to be associated with bouts of strong directional selection [14]. Related lineages of livebearing fishes have independently adapted to two extreme environmental factors: toxic hydrogen sulphide (H2S) and perpetual darkness. We asked at which points during development changes in the timing of the involved processes (i.e., heterochrony) would be detectible
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