Phylogeny of denticulate catfish (Loricarioidei: Siluriformes) and their use as a new model to understand the evolution and development of dental tissue in new areas of the vertebrate body

Abstract

Dental structures originally emerged as components of the exoskeleton of ancestral vertebrates. Throughout evolution, these structures started being built inside the oral cavity, allowing these ancestral vertebrates to switch to a more predatory lifestyle and opening a vast diversity of new ecological niches. However, to date, the evolutionary and developmental processes by which dental structures can be built in new areas of the body plan are not clear. One of the main limitations for investigating this question is the lack of informative model organisms that show a clear gain of dental structures in new areas of the body. In this study, I focus my studies on catfish (Teleostei: Silurifomes): a highly diverse group of fish that contains a lineage of denticulate catfish (Loricarioidei) in which dental structures presumably emerged de novo on extra-oral body surfaces. I use the Loricarioidei to study the evolutionary and developmental mechanisms through which dentition can be built in new areas of the vertebrate body plan. Because this lineage has never been studied in the context of dental evolution, I must take a multidisciplinary approach at this question to have a broad perspective of the factors related to the gain of dental structures in the loricarioid body. In this work I integrate information that I recovered through studies in the fields of molecular phylogenetics, morphology, evolutionary biology and developmental biology. I begin by determining the phylogenetic landscape in which these denticles emerged, and start by placing the Loricarioidei within the catfish phylogeny. However, the fast molecular evolution of this group and the general diversity of evolutionary rates among catfish species raise methodological challenges for inferring this phylogeny correctly. I address these challenges and propose two new methods, LS³ and LS⁴, to improve any phylogeny inference in which extreme heterogeneous evolutionary rates may be a source of bias. I apply LS⁴ as implemented in a software I produced for this work, LSX, on a new molecular dataset to address the position of the Loricarioidei, and I am able to place this lineage nested within Siluriformes, among groups of catfish that have a naked skin. These results confirm that dental structures indeed emerged de novo in the extra-oral regions of loricarioids. I then ask if the evolutionary emergence of the loricarioid denticles was linked to the formation of other bony elements observed in this lineage, such as dermal bony plates. Through ancestral state reconstruction, I find that the emergence of loricarioid denticles was not linked in evolution to the emergence of dermal bony plates, but that an underlying superficial bone is likely essential for the formation of these dental structures. In the final section of this work I enter into the developmental mechanisms through which these de novo dental structures are built. I use the species Ancistrus triradiatus, which is the new model loricarioid catfish species developed in the laboratory of Juan Montoya-Burgos. Through in situ hybridization and immunostaining studies, I find that loricarioid denticles, despite being an independent emergence of dental structures in new body areas, are produced by deploying the same developmental genetic program that produces oral teeth in other vertebrates. This indicates that dental structures found inside and outside the oral cavity in this loricarioid model species are homologous. In view of these results I conclude that it is possible for vertebrates to gain dental structures in new areas of the body through the cooption of the oral tooth developmental program.