Evolution of acoustic communication in European gobies (Gobius lineage) based on molecular markers

• ¹ Faculty of Science, University of Zagreb, Croatia
• ² Università Ca' Foscari, Italy

Animal acoustic communication is an important behavioral feature that allows individuals to exchange inter and intraspecific information about their location, territory, condition, sex, etc. Closely related species are predicted to have similar sounds due to the shared ancestry of the behavior and morphology of sound-producing mechanism. Within the acoustic communication system, mating signals provide useful information about an individual's reproductive layout and as such is directly involved in mate choice. In addition, by being involved in mate attraction (and choice), mating signals are under strong sexual selection, which could lead to rapid divergence or even speciation in different groups. Gobies (Gobiiformes; Gobioidei) are the most diverse fish family within European ichthyofauna, comprising about one-tenth of all Mediterranean fish biodiversity. They have a worldwide distribution and show a spectacular variety in morphology, ecology, and behavior. In addition, their systematic and phylogenetic relationships are still unresolved. From an acoustic point of view, gobies are one of the best-studied vocal fish group, but a still small proportion of species have been acoustically tested. They produce sound during aggressive or reproductive intraspecific interactions, and mating sounds are important since they increase the fitness of the soniferous individuals. Therefore, it is assumed that the sound parameters could carry a phylogenetic signal. By using phylogenetic reconstruction methods and statistical approach, herein we investigated the sound evolution in nine European gobies from Gobius lineage (genus Padogobius, Neogobius, Ponticola, Gobius, and Zosterisessor). We constructed phylogenetic trees from sequence data of two molecular markers (RAG and cytb) and compared the pattern of diversification with bioacoustics data. In addition, we quantitatively compared the sounds produced by the males from nine Gobius lineage species according to their acoustic variables, both temporal and spectral. In addition, we included ancestral soniferous gobioid to serve as a gobiiform outgroup (Perccottus glenii) aiming to build well-supported phylogeny of acoustic communication in gobiids (Gobius lineage). Deep structuring and significant diversity is present within most of Gobius lineages, explained by differences in habitats, but also long-term and complex evolutionary history. Multivariate statistics combining acoustic parameters and genetic analysis showed that gobies from Gobius lineage were separated into two groups, Ponto-Caspian and Atlantic-Mediterranean. Ponto-Caspian species produced exclusively tonal sounds which were spectro-temporally modified (long or short in duration with frequency modulation). Conversely, Atlantic-Mediterranean gobies were characterized with more diverse vocal repertoire, with some species (P. bonelli) producing three different sound types (tonal, pulsatile and complex). Furthermore, our results indicate that species from Padogobius genus correspond to different groups, both genetically and acoustically. On the phylogenetic tree, P. bonelli was placed more closely to Gobius species, while P. nigricans was situated inside Neogobius group. These results indicate that genus Padogobius could be paraphyletic. In addition, we demonstrate sound production has basal origin within gobioids, since Perccottus glenii, basal odotobutid, was able to produce two different sounds types (thumps and tonal sounds). Therefore, we hypothesize that sound communication could be a synapomorphic trait for gobioid fishes. Recent taxonomy is not completely concordant with molecular phylogeny and cryptic diversity is present. Our analysis presents the comprehensive attempt of using DNA sequences and bioacoustics traits in constructing phylogenetic scenario aiming to explain the pattern of acoustic evolution in gobies.