Biogeography, phylogenetics, and cryptic species in the Myobatrachid frog genus Uperoleia

Abstract

My thesis concerns the evolutionary history of the endemic Austro-Papuan frog genus Uperoleia (Family Myobatrachidae). I use a molecular phylogenetic approach, in conjunction with ecological and palaeoclimate modelling, to evaluate and describe true Uperoleia diversity, and to understand how this diversity relates to historic and contemporary landscape history. As the majority of Uperoleia species are distributed in the Australian Monsoonal tropics, much of this thesis focuses on Northern Australia.

Studies of Australian monsoonal tropics biogeography are in their infancy. For species active in the wet season, including frogs, the remoteness and inaccessibility of this massive region has made studies inherently difficult. Researchers are still working to understand patterns of species distributions and the barriers and mechanisms that have shaped them. Due in part to its vast size, huge variation exists in sub-region climate patterns in the monsoonal tropics, which is driven in part by strong topological complexity, especially compared to the adjacent desert regions. Do species within biomes form monophyletic groups? What factors have driven between-biome diversification? What are the patterns of within-biome phylogeography? What role has the aridification of the Australian continent played in shaping the evolutionary histories of mesic-adapted taxa? These were the questions that I sought to address in my thesis. In doing so, I uncover patterns of mitochondrial introgression, and explore the possible influence of hybridization on diversification in this group of frogs.

The first chapter of my thesis investigates the diversity and distribution of Uperoleia species in the arid zone of Australia. The dunefield deserts of Australia are particularly poorly explored for frogs. In order to understand patterns of diversification between the monsoonal tropics and the arid zone, systematics of arid zone Uperoleia needed to be resolved. Using a combination of molecular genetics, morphological data, and acoustic data, I found that five species were present in the arid zone, rather than the previously described three. In this chapter I redescribe four of these species, as well as a new species only found in the Pilbara. The high level of arid zone diversity and distinct distribution patterns indicated that the topographic complexity creates strong patterns of sub-region endemism.

Chapter II explores monsoonal tropics biogeography using a widespread clade of Uperoleia that span the entire region. Using multiple mitochondrial and nuclear loci, I generated a well-resolved phylogeny. Despite numerous instances of mitochondrial introgression, morphological and acoustic data allowed me to resolve the species distributions of four parapatric species. Using distribution and environmental data, combined with climate modelling, I generated species distribution models to explore the biogeographic barriers influencing the patterns of present day species. These data allowed me to revise the biogeographic terminology related to the Australian monsoonal tropics and propose new barriers within the region. In addition, I project the current niche space back to the Last Glacial Maximum (21 kya) in order to identifY putative refugia. These refugia largely match the population structure we see today.

In Chapter III, I resolve the systematics of U. trachyderma using the molecular genetic, morphological, and acoustic data from Chapter II. The previous chapter concluded that there is sufficient evidence to conclude that individuals from the western half of the Northern Deserts are reproductively isolated from U. trachyderma, and in this chapter I resolve the systematics with the description U. stridera sp. nov., and the re-description of U. trachyderma. Due to increasing evidence that the Northern Deserts region of Australia harbours a unique fauna, I also discuss the status of protected areas within the Northern Deserts.

In Chapter IV, I generate a multi-locus molecular data set for almost 600 specimens to provide a comprehensive assessment of Uperoleia phylogeny and clarify the distributions of 25 of the 28 Uperoleia species. I then investigate phylogeographic structure within each of the arid, monsoonal tropic, and mesic biomes, and the timing and patterns of between-biome diversification. I provide a detailed review of the geology, landscape and climate patterns that may have influenced current species distributions and contrast these with previous studies. For the eastern mesic zone, species distribution patterns are largely congruent with previous phylogeographic studies. Examination of molecular dates revealed the divergence between an eastern mesic clade and a largely monsoonal tropics clade was associated with the peak of the wann, wet Miocene epoch. It also appears that species have diverged into the arid zone from the monsoonal tropics multiple times. The majority of these divergence events coincide with the peak of the Pliocene, which saw warmer wetter conditions in central Australia. The divergence between the most arid-adapted taxa and its monsoonal sister species was associated with the beginning of the Pleistocene and beginning of the intense aridification of central Australia.

Chapter V addresses the topological differences between the mitochondrial and nuclear phylogenies of Uperoleia. Here I make the case that due to chromosomal conservatism, and evidence of recent and regular hybridization, it is possible that homoploid hybrid speciation played a role in the generation of diversity. Although patterns such as deep coalescence and mitochondrial gene capture may also explain some topological differences, ecological changes associated with potential hybrid species mean further investigations are necessary. Consideration of heterozygosity in the nuclear markers, and next-gen sequencing are the way forward for understanding tree discordance in Uperoleia.