Complexity of Interrelationship Between Astyanax Cave and Surface Fish

Abstract

The haplotype distribution of the Astyanax surface fish and the origin of its cave forms is strongly influenced by Pleistocene climatic change, due to which large-scale extinction and recolonization by the surface fish took place. Because of this history and the persisting interfertility, the relationship between the Astyanax strongly eye- and pigment-reduced (SEP) and variably eye- and pigment-reduced (VEP) cave populations as well as the recent surface populations is very complex. Although based on nuclear genes clustering with the phylogenetically old SEP, the Pachon and Yerbaniz cave populations are exceptional and show close relationship to both the recent surface and the phylogenetically young VEP cave fish due to mitochondrial capture. Furthermore, the variability of eye size observed in the VEP, especially in the Chica cave population, was often explained by hybridization. This contrasts with the finding that no gene flow exists in the SEP Yerbaniz and VEP Micos cave fish populations, where cave and starved surface fish co-occur. This is explained by the surface fish being washed into the caves and not being able to compete with the well adapted SEP or VEP cave fish in darkness. These observations are in accordance with Gause’s Law which predicts that two ecomorphs competing for the same resource cannot coexist in the same niche. In the cave habitat the cave fish are at an advantage, which will finally lead to the extinction of the surface specimens competing for food. This process is reinforced in the Astyanax caves every year by periodic low food supply outside the rainy seasons. Bottlenecking obviously regularly occurs, which is demonstrated by the low variability of several genetic markers compared with the surface fish. However, mitochondrial introgression in the SEP cave populations like Pachon and Yerbaniz has nonetheless occurred. It is suggested that the introgressed modern haplotypes in the SEP Pachon and Yerbaniz cave fish derive from VEP cave populations, which, like the recent VEP Micos cave fish, were well adapted to cave life and therefore able to co-exist and also to hybridize with the SEP cave populations after the cave systems merged due to karst erosion. The recent surface fish on the one hand and the SEP and VEP cave populations on the other no longer hybridize in nature. In accordance with the Biological Species Concept, the SEP and VEP cave populations therefore can be denominated as a species on their own. The cave fish speciation process provides one of the rare examples of parallel speciation.