Phylogeny and divergence ages in Crocodylia: implications for crown-clades and paleobiogeography

Abstract

Crocodylia is represented by semi-aquatic ambush predators that inhabit freshwater and estuarine environments in the tropical and subtropical regions of the globe. Composed by 25 extant recognized species in three main lineages (Crocodyloidea, Gavialoidea and Alligatoroidea), mitogenomic studies recognizes a higher diversity of crocodylians within cryptic species complexes that are otherwise unrecognizable based on morphological analyses. Extinct crocodylian species furthermore outnumber the living diversity as evidenced by a considerable fossil record extending to late Stages of the Cretaceous Period. The combination of well sampled fossil record and low extant diversity that allows comprehensive sampling for molecular data makes Crocodylia a good model clade for macroevolutionary studies. In spite of phylogenetic analysis using molecular data consistently recover a common topology, paleontological studies in Crocodylia often continue to use morphology-only datasets, which in turn impacts on on the inferred phylogenetic position of many fossil taxa. Examples of topological discrepancies in Crocodylia are represented by: (i) the phylogenetic position of the Indian gharial Gavialis gangeticus represents one of the long-standing conflicts in crocodylian systematics, as phylogenetic inferences based on morphology alone places Gavialis sister to all other living crocodilians (i.e. alligators and crocodiles), whereas molecular data unite Gavialis with the false gharial Tomistoma schlegelii as a sister clade to Crocodylidae alone. These topological discrepancies in turn affects particularly taxa close to the root of Crocodylia and/or with a Gavialis-like morphology. Hence, the ambiguous phylogenetic position of basal fossil taxa may eventually lead to unreasonable selection of fossil calibrations for divergence age estimates in molecular studies, which in turn majorly affects macroevolutionary inferences in Crocodylia; (ii) Similarly, topological conflicts are furthermore observed in the crown clades of Alligatoridae (Caimaninae, Alligatorinae), as incomplete fossil and unstable phylogenies of extinct caimanines hamper a reconstruction of early evolution in the clade, in addition to poorly justified selection of fossil as calibration in molecular studies overestimate the origin of total and crown-Caimaninae; and finally (iii) the origin of the Chinese alligator (A. sinensis) is considered a biogeographical puzzle, as the timing and climatic context of Alligator dispersal from North America to Asia is poorly constrained: paleontological evidence and molecular estimates for the split between A. sinensis and its only closest living relative A. mississippiensis (American alligator) are in conflict; Alligator fossils have never been recovered in the stem-lineage of A. sinensis; and Alligator fossil species from Asia have never been included into a phylogenetic framework. In the present thesis, in order to investigate the three abovementioned conflicts in crocodylian systematics, I explore (I) the effects of the use of molecular data on the position of fossil taxa close to the root of Crocodylia; (II) the phylogeny of Caimaninae as an extensive reappraisal of the position of fossil taxa in addition to provide well-justified fossil calibrations for the total and crown-groups; (III) the evolution of Alligator focusing on expanding the dataset by describing a new Alligator species, Alligator munensis, and by including fossil species from Asia into a phylogenetic context, contributing to the understanding of Alligator intercontinental dispersal. A series of methodologies were explored in order to meet the objectives, including traditional alpha-taxonomy descriptions, use of computed tomography, extensive literature review, phylogenetic analysis under Maximum Parsimony, undated Bayesian inference and total evidence tip dating. The studies composing this thesis contribute significantly for the comprehension crocodylian systematics by providing time-scaled phylogenies, highlighting the importance of DNA-informed phylogenetic inference for basal crocodylian relationships and divergence age estimates together with the use of well-justified fossil calibrations, and contributes to the understanding of Alligator evolution and biogeography.