Evolution and diversification of a sexually dimorphic luminescent system in ponyfishes (Teleostei: Leiognathidae), including diagnoses for two new genera.

Abstract

A phylogeny was generated for Leiognathidae, an assemblage of bioluminescent, Indo-Pacific schooling fishes, using 6175 characters derived from seven mitochondrial genes (16S, COI, ND4, ND5, tRNA-His, tRNA-Ser, tRNA-Leu), two nuclear genes (28S, histone H3), and 15 morphological transformations corresponding to features of the fishes' sexually dimorphic light-organ system (LOS; e.g., circumesophageal light organ, lateral lining of the gas bladder, transparent flank and opercular patches). Leiognathidae comprises three genera, Gazza, Leiognathus, and Secutor. Our results demonstrate that Leiognathidae, Gazza, and Secutor are monophyletic, whereas Leiognathus is not. The recovered pattern of relationships reveals that a structurally complex, strongly sexually dimorphic and highly variable species-specific light organ is derived from a comparatively simple non-dimorphic structure, and that evolution of other sexually dimorphic internal and external features of the male LOS are closely linked with these light-organ modifications. Our results demonstrate the utility of LOS features, both for recovering phylogeny and resolving taxonomic issues in a clade whose members otherwise exhibit little morphological variation. We diagnose two new leiognathid genera, Photopectoralis and Photoplagios, on the basis of these apomorphic LOS features and also present derived features of the LOS to diagnose several additional leiognathid clades, including Gazza and Secutor. Furthermore, we show that five distinct and highly specialized morphologies for male-specific lateral luminescence signaling, which exhibit species-specific variation in structure, have evolved in these otherwise outwardly conservative fishes. Leiognathids inhabit turbid coastal waters with poor visibility and are often captured in mixed assemblages of several species. We hypothesize that the species-specific, sexually dimorphic internal and external modifications of the leiognathid LOS provide compelling evidence for an assortative mating scheme in which males use species-specific patterns of lateral luminescence signaling to attract mates, and that this system functions to maintain reproductive isolation in these turbid coastal environments.