From dragons to master genes. A journey through the ideas on the evolution of cave animals

Abstract

The beginnings of a systematic research on cave biology date from the early XX Century, when Emil G. Racovitza sparked off the spectacular rise of modern biospeleology in Europe. In the mid XX Century, considerable progress was achieved in the domains of taxonomy, ecology and physiology of European and North American cave faunas, and data available were summarized in two key monographs: Albert Vandel’s Biospéologie (1964) and Thomas C. Barr’s Cave ecology and the evolution of troglobites (1968). In the 1970 decade, the first population genetics studies, using gel electrophoresis approaches, were published. Later, discoveries of rich cave faunas in tropical caves resulted in new breakthroughs in our understanding of cave colonization and evolution of troglobites. In general, the troglobiomorphic features of fully adapted cave animals (depigmentation, anophtalmy, proliferation of sensory devices) were considered adaptations for surviving in extreme conditions of darkness and limited energy supplies. The gain of useful structures (proliferation of sensory devices in longer and more slender appendages) was easily explained with natural selection arguments, but the loss of eyes and pigmentation was more difficult to explain. The discovery of troglobites in tropical caves, which had much less energetic limitations, often showed less pronounced troglobiomorph features, which come to support the hypothesis that energy required to make eyes and pigments was the limiting factor. In any case, the forces governing regressive evolution remained under debate between neutralists and selectionists, being the loss of eyes the most paradigmatic case study. In Europe, the German School initiated by Curt Kosswig is presently followed by Horst Wilkens and their studies on the evolution of regressive characters using the cave fish Astyanax mexicanus as research subject. Wilkens maintains that regressive evolution is driven by mutation and genetic drift processes, in which mutations that would be destructive in a surface population (affecting eye function) are not eliminated in a cave population. The American School initiated by Thomas Barr is presently followed by William Jeffery and their studies on the evolution of regressive characters also using the cave fish Astyanax mexicanus . Jeffery claims that gene products that promote eye development may be detrimental to the development of positive characters of cave animals. Thus, eye loss in a cave population leads to an increase of traits that improve life in darkness in this population . The debate is still alive.