Abstract
Cynopoecilines comprise a diversified clade of small killifishes occurring in the Atlantic Forest, one of the most endangered biodiversity hotspots in the world. They are found in temporary pools of savannah-like and dense forest habitats, and most of them are highly threatened with extinction if not already extinct. The greatest gap in our knowledge of cynopoecilines stems from the absence of an integrative approach incorporating molecular phylogenetic data of species still found in their habitats with phylogenetic data taken from the rare and possibly extinct species without accessible molecular information. An integrative analysis combining 115 morphological characters with a multigene dataset of 2,108 bp comprising three nuclear loci (GLYT1, ENC1, Rho), provided a robust phylogeny of cynopoeciline killifishes, which was herein used to attain an accurate phylogenetic placement of nearly extinct species. The analysis indicates that the most recent common ancestor of the Cynopoecilini lived in open vegetation habitats of the Atlantic Forest of eastern Brazil and was a miniature species, reaching between 25 and 28 mm of standard length. The rare cases of cynopoecilines specialized in inhabiting pools within dense forests are interpreted as derived from four independent evolutionary events. Shifts in habitat usage and biogeographic patterns are tentatively associated to Cenozoic paleogeographic events, but the evolutionary history of cynopoecilines may be partially lost by a combination of poor past sampling and recent habitat decline. A sharp evolutionary shift directed to increased body size in a clade encompassing the genera Campellolebias and Cynopoecilus may be related to a parallel acquisition of an internally-fertilizing reproductive strategy, unique among aplocheiloid killifishes. This study reinforces the importance of adding morphological information to molecular databases as a tool to understand the biological complexity of organisms under intense pressure from loss of habitat.
Highlights
The Atlantic Forest of eastern Brazil has been known since the nineteen century for its rich diversity of animal and plant species [1, 2, 3], and is placed among the five most important biodiversity hotspots in the world [4]
Among fish groups endemic to the Atlantic Forest, the aplocheiloid killifish tribe Cynopoecilini is remarkable for including among its members the smallest and most colourful fish species of the biome, as well as standing among the vertebrates most threatened with extinction in the Neotropical region [10, 11]
The resulting tree topology indicates relationships differing from that indicated in previous studies [15, 20, 21, 22], including Mucurilebias leitaoi as the sister group to a clade comprising all other cynopoecilines and Leptolebias marmoratus as the sister group to a clade comprising Campellolebias and Cynopoecilus
Summary
The Atlantic Forest of eastern Brazil has been known since the nineteen century for its rich diversity of animal and plant species [1, 2, 3], and is placed among the five most important biodiversity hotspots in the world [4]. Most cynopoecilines are endemics of the Atlantic Forest, but a few species are found in the adjacent grass areas of southern Brazil and northeastern Uruguay [12]. Fish die but eggs survive in embryonic diapause stage buried in the bottom substrate until the rainy season [10]. Killifishes adopting this uncommon life cycle have been called annual killifishes, i.e., having a single generation by year [13]. Cynopoecilines are quite specialised in habitat use, with some species found in open vegetation savannah-like areas and others restricted to dense forest habitats, as described below
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