Molecular investigations of the pteroinae : insights into the invasive lionfishes from the native range

Abstract

The lionfishes (subfamily Pteroinae) are among the most visually distinctive fishes in the world. Their long, venomous spines have made them extraordinarily popular in the aquarium trade, but unfortunately, such popularity has led to their introduction outside their native range, where they have become highly invasive. Prior to the invasion of lionfish into the Atlantic, Caribbean and Gulf of Mexico, little was known about the pteroids. Research has begun to fill in gaps in our understanding of their biology and ecology, but it is hampered by a lack of evolutionary context. The goal of my dissertation was to use molecular methods to investigate this well-known but understudied group, including a phylogenetic examination of the subfamily and studies of their known protein toxins using genetic and proteomic approaches. Initial construction of a Pteroinae phylogeny revealed more diversity at the genus level than currently recognized by taxonomy. Results from Bayesian analyses suggest the five genera are more appropriately split into eight. Similarly, toxin gene sequences suggest higher inter-and intraspecific diversity in the main venom protein than previously known. The high degree of divergence was linked to positive selection acting upon toxin genes, among the first evidence for the role of strong positive selective forces in shaping defensive venoms. Phylogenetic reconstruction indicated the need for further investigation of the relationships between four putative lionfish species: the two invasive species Pterois volitans and P. miles and two closely related congeners, P. lunulata and P. russelii. Phylogeographic analyses revealed only two major lineages within the four species: an Indian Ocean lineage consisting largely of P.miles, and a Pacific Ocean lineage consisting largely of P. lunulata and P. russelii. Specimens taxonomically identified as P. volitans appeared to be hybrids between the two lineages, possessing alleles from both lineages and intermediate phenotypes at key distinguishing meristic characters. The degree and extent of hybridization suggests that the two lineages may not be separate species, and currently recognized taxonomy instead reflects phenotypic variation within a single, wide-ranging, polytypic species or the potential formation of a hybrid swarm stemming from secondary contact and changes to oceanic biogeographic barriers over the last 2 million years. Finally, investigations of venom protein expression revealed that putative toxins are present in diverse tissues in lionfish. These toxins were found even in lipophilic extracts of tissues, suggesting potential contamination of ciguatoxin assays may be occurring. Together, the data from the three data-driven chapters have key implications for management practices, and point to important avenues for further research to truly understand these dangerous but beautiful fishes.