Extreme gender flexibility: Using a phylogenetic framework to infer the evolution of variation in sex allocation, phylogeography, and speciation in a genus of bidirectional sex changing fishes (Lythrypnus, Gobiidae)

The genus Lythrypnus is a group of marine gobies that exhibit extreme gender flexibility as bidirectional sex changers. The genus consists of 20 described species and several undescribed species that are distributed in the Americas. Five species have been characterized with respect to sex allocation and gonad morphology. The hormonal, morphological, and behavioral aspects of sex change have been studied extensively for one species, L. dalli. These data, however, have not been interpreted in an evolutionary context because a phylogenetic hypothesis has not previously been proposed for the genus Lythrypnus. We propose the first phylogenetic hypothesis for the genus based on molecular data from three mitochondrial genes (12s, ND2, and Cytb), one nuclear gene (Rag1) and one nuclear intron (S7). We also include three previously undescribed Lythrypnus species. Our results support the monophyly of the genus with L. heterochroma, an Atlantic species, as the basal taxon. After the divergence of L. heterochroma, there are two main clades, one comprised of species distributed in the Atlantic, the other comprised of species distributed in the Pacific. These data indicate an Atlantic origin for the genus, followed by divergence after the closure of the Isthmus of Panama. Our data also support the monophyly of three previously described species complexes, the L. rhizophora complex and L. dalli complex in the Pacific, and the L. mowbrayi complex in the Atlantic. We mapped patterns of sex allocation within this genus onto the fully resolved and supported topology, and found that sexual plasticity and gender flexibility is likely a synapomorphy for the genus. Overall our results create a well-supported framework to understand the phylogeography of the genus, and to interpret the evolution of sex allocation in Lythrypnus gobies.

Graphical abstractFigure optionsDownload full-size imageDownload as PowerPoint slideHighlights► In this paper we propose a phylogeny for a genus of bidirectionally sex changing fishes, Lythrypnus. ► Sequence three mitochondrial genes (Cytb, 12s, and ND2) one nuclear gene (Rag1) and a nuclear intron (S7). ► We investigate the evolution of sex allocation within the genus. ► Phylogeny revealed one major split into an Atlantic and a Pacific clade separate by the Isthmus of Panama. ► No trends in sex allocation variation were inferred from common ancestry.