Taxonomy, ecology and conservation genomics of North-Eastern Australian Earless Dragons (Agamidae: Tympanocryptis spp.)

Abstract

Land clearing and modification of natural habitats is threatening biodiversity globally. In Australia, most native grassland habitats have been heavily modified for agriculture, including cropping and grazing. Grassland specialist species, including earless dragon lizards (Tympanocryptis spp.) in north-eastern Australia, are of conservation concern due to this continued habitat loss and fragmentation. However, the north-eastern Australian group of earless dragons (including the recently described T. condaminensis, T. wilsoni and T. pentalineata) are at significant risk, due to the presence of multiple undescribed cryptic Tympanocryptis lineages within this region. It is imperative that the taxonomy is resolved for these cryptic lineages of conservation concern, so conservation of these species may occur.

One of the major challenges for taxonomists in recent times has been the species delimitation of morphologically cryptic taxa. The detection of distinct molecular lineages within cryptic genera has increased exponentially over the past decades with advances in genetic techniques. However, there are discrepancies in the rate and success of detection of cryptic taxa between studies using genetic methods and those using classic external morphology analyses. Therefore, novel integrative methods for species delimitation of cryptic taxa provide an avenue to incorporate multiple lines of evidence, including the application of osteological variation assessment where external morphological assessment fails to distinguish species. I develop a new pipeline integrating genomic data using single nucleotide polymorphisms (SNPs) and osteological geometric morphometric evidence from micro X-ray computed tomography (CT) imagery to assess variation between cryptic lineages for confident species delimitation.

Here, I use this novel integrative pipeline to delimit cryptic lineages of earless dragons in north-eastern Australia. Prior to this study, there was evidence of three undescribed species of Tympanocryptis in this region. Using single mitochondrial and nuclear genes along with >8500 SNPs, I assess the evolutionary independence of the three target lineages and several closely related species. I then integrate these phylogenomic data with osteological cranial variation from CT imagery between lineages. I find that the very high levels of genomic differentiation between the three target lineages is also supported by significant osteological differences between lineages. By incorporating multiple lines of evidence for species delimitation, I provide strong support that the three cryptic lineages of Tympanocryptis in north-eastern Australia warrant taxonomic review.

Earless dragons are found in most environments across the Australian continent, including a variety of ecological niches, from stony desert to tropical woodland or cracking clay savannah, although each species is often restricted to s certain habitat-type. I investigate the phylogenetic relationships among currently described earless dragons and newly delimited putative species with an assessment of broad biogeographic divisions, focussing on the north-eastern Australian Tympanocryptis group. I found significant structure across the north-eastern Australian lineages, with deep divergence between lineages occurring in the inland Great Artesian Basin region and more coastal Great Dividing Range. Regional diversification is estimated to have occurred in the late Miocene with subsequent Plio-Pleistocene speciations, and divergence and distributions of these species may therefore be reflective of the climate induced grassland-rainforest oscillations during this time. Based on these phylogenetic geographic relationships and the species delimitation from the integrative taxonomy approach, I describe three new species of Tympanocryptis from the cracking clay grasslands of the Darling Riverine Basin (T. darlingensis sp. nov.) and Queensland Central Highlands (T. hobsoni sp. nov.), and the stony open eucalypt woodlands on the Einasleigh Uplands (T. einasleighensis sp. nov.). The revision of these species provides further taxonomic clarity within the Tympanocryptis genus, and is an imperative step in the conservation of the north-eastern Australian earless dragons.

These three putative Tympanocryptis species and the other three recently described earless dragons in north-eastern Australia inhabit restricted niches and areas with varying levels of habitat fragmentation and modification, and are therefore of significant conservation concern. However, little is known about these six north-eastern Australian earless dragon species. I utilise genomic methods to investigate population connectivity and genetic structure to determine management units. I then use species distribution modelling (SDM) to assess habitat suitability and fragmentation of each species. I integrate results of these analyses to form conclusions on the distribution and population structure of these earless dragons. I then discuss the major threatening processes and potential conservation strategies.

This thesis uses several integrative approaches in resolving the taxonomy and forming conclusions on the conservation management of the north-eastern Australian Tympanocryptis species. This study successfully delimits cryptic lineages, explores the phylogenetic and geographic relationships between species, and provides baseline population genomics and ecological data to be used for conservation assessments and management decisions of earless dragons in north-eastern Australia.