Evolution of a hotspot genus: geographic variation in speciation and extinction rates in Banksia (Proteaceae)

BACKGROUND: Hotspots of angiosperm species richness and endemism in Mediterranean-climate regions are among the most striking, but least well-understood, geographic patterns of biodiversity. Recent studies have emphasized the importance of rapid diversification within hotspots, compared to non-hotspot regions, as a major contributor to these patterns. We constructed the first near-complete phylogeny of Banksia (Proteaceae) to test whether diversification rates have differed between lineages confined to the southwest Australian hotspot and those found throughout southern, eastern and northern Australia. We then tested for variation in diversification rates among the bioclimatic zones within the southwest hotspot itself. RESULTS: Although Banksia species richness in the southwest is ten times that of the rest of the continent, we find little evidence for more rapid diversification in the southwest, although this result is inconclusive. However, we find firmer support for substantial rate variation within the southwest hotspot, with more rapid diversification in the semi-arid heaths and shrublands, compared to the high-rainfall forests. Most of the Banksia diversity of the southwest appears to be generated in the heaths and shrublands, with a high migration rate out of this zone boosting diversity of the adjacent forest zone. CONCLUSIONS: The geographic pattern of diversification in Banksia appears more complex than can be characterized by a simple hotspot vs. non-hotspot comparison, but in general, these findings contrast with the view that the high diversity of Mediterranean hotspots is underpinned by rapid radiations. Steady accumulation of species at unexceptional rates, but over long periods of time, may also have contributed substantially to the great botanical richness of these regions

Evolution of a hotspot genus: geographic variation in speciation and extinction rates in Banksia (Proteaceae)

BACKGROUND Hotspots of angiosperm species richness and endemism in Mediterranean-climate regions are among the most striking, but least well-understood, geographic patterns of biodiversity. Recent studies have emphasized the importance of rapid diversification within hotspots, compared to non-hotspot regions, as a major contributor to these patterns. We constructed the first near-complete phylogeny of Banksia (Proteaceae) to test whether diversification rates have differed between lineages confined to the southwest Australian hotspot and those found throughout southern, eastern and northern Australia. We then tested for variation in diversification rates among the bioclimatic zones within the southwest hotspot itself. RESULTS Although Banksia species richness in the southwest is ten times that of the rest of the continent, we find little evidence for more rapid diversification in the southwest, although this result is inconclusive. However, we find firmer support for substantial rate variation within the southwest hotspot, with more rapid diversification in the semi-arid heaths and shrublands, compared to the high-rainfall forests. Most of the Banksia diversity of the southwest appears to be generated in the heaths and shrublands, with a high migration rate out of this zone boosting diversity of the adjacent forest zone. CONCLUSIONS The geographic pattern of diversification in Banksia appears more complex than can be characterized by a simple hotspot vs. non-hotspot comparison, but in general, these findings contrast with the view that the high diversity of Mediterranean hotspots is underpinned by rapid radiations. Steady accumulation of species at unexceptional rates, but over long periods of time, may also have contributed substantially to the great botanical richness of these regions.The work was funded by an Australian Research Council Discovery Grant and QEII Fellowship to M. Cardillo (DP0879971), with additional funding provided by the Research School of Biology at the Australian National University

Inferring Kangaroo Phylogeny from Incongruent Nuclear and Mitochondrial Genes

The marsupial genus Macropus includes three subgenera, the familiar large grazing kangaroos and wallaroos of M. (Macropus) and M. (Osphranter), as well as the smaller mixed grazing/browsing wallabies of M. (Notamacropus). A recent study of five concatenated nuclear genes recommended subsuming the predominantly browsing Wallabia bicolor (swamp wallaby) into Macropus. To further examine this proposal we sequenced partial mitochondrial genomes for kangaroos and wallabies. These sequences strongly favour the morphological placement of W. bicolor as sister to Macropus, although place M. irma (black-gloved wallaby) within M. (Osphranter) rather than as expected, with M. (Notamacropus). Species tree estimation from separately analysed mitochondrial and nuclear genes favours retaining Macropus and Wallabia as separate genera. A simulation study finds that incomplete lineage sorting among nuclear genes is a plausible explanation for incongruence with the mitochondrial placement of W. bicolor, while mitochondrial introgression from a wallaroo into M. irma is the deepest such event identified in marsupials. Similar such coalescent simulations for interpreting gene tree conflicts will increase in both relevance and statistical power as species-level phylogenetics enters the genomic age. Ecological considerations in turn, hint at a role for selection in accelerating the fixation of introgressed or incompletely sorted loci. More generally the inclusion of the mitochondrial sequences substantially enhanced phylogenetic resolution. However, we caution that the evolutionary dynamics that enhance mitochondria as speciation indicators in the presence of incomplete lineage sorting may also render them especially susceptible to introgression.This work has been supported by Australian Research Council grants to MJP (DP07745015) and MB (FT0991741). The website for the funder is www.arc.gov.au. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript

Patterns and processes in animal evolution : molecular phylogenetics of Southern Hemisphere fauna : a thesis presented in partial fulfilment of the requirements for the degree of Doctor of Philosophy in Genetics

Three kinds of processes are known to modify the geographical spatial arrangement of organisms: dispersal, extinction and vicariance. The Southern Hemisphere has an intriguing and complicated geological history that provides an ideal backdrop to study these processes. This thesis focuses on three historical events that illustrate these processes: the proposed marine inundation of New Zealand in the Oligocene, the asteroid impact at the K – Pg boundary, and the continental breakup of Gondwana. It investigates what impact these events had on species diversification by studying the phylogenetic relationships of two groups of taxa – the family Anostostomatidae (insects), and Neoaves (birds). Anostostomatidae were studied in relation to the Oligocene drowning and the break up of Gondwana as they have a wide southern distribution, found on all “Gondwanan” fragments with the exception of Antarctica, and are thought represent an ancient lineage that predates the Gondwanan breakup. Birds, in particular Neoaves, were studied in relation to the asteroid impact at the K – Pg boundary. Although birds are mobile and many circumnavigate the globe between seasons, they are suggested to have originated in the Southern Hemisphere in Gondwanan times, and subsequently undergone range expansion and diversification around the world. In order to address the relationship (if any) between modern biotic diversity and historical geological events, phylogenetic relationships were determined and where possible, molecular clock analysis carried out. Timing information provided by molecular clock analysis is important as it enables distinction between opposing hypotheses such as vicariance and dispersal. In Chapter Two, the phylogenetic relationships within the family Anostostomatidae are investigated. One of the most controversial times in New Zealand’s geological history is during the Oligocene. Some suggest that the lack of fossils and evidence for recent dispersal of numerous taxa support the notion that all modern biota reached the region during the last 25 million years. Anostostomatidae were chosen as they represent a group of insects that are thought to be ancient and there is little published data in the literature. Previous studies focused on the relationships within Hemideina and Deinacrida suggesting that these groups diversified in the early Miocene. The data presented here are from mitochondrial (COI and 12S) and nuclear (18S and 28S) sequences. Molecular dating using a relaxed clock as implemented in BEAST suggest that in fact some lineages were present at or shortly after continental breakup and could have survived throughout this turbulent time. As there were no definitive fossils to use for calibration points, geological events were used as calibration points for the molecular clock. Mutation rates obtained from the different analyses were compared to those published for other insects in an attempt to identify the most likely model. Both maximum likelihood and Bayesian analyses support the presence of three distinct ecological groups in New Zealand; Hemiandrus (ground weta), Anisoura/Motuweta (tusked weta) and Hemideina–Deinacrida (tree–giant weta). With regards to their Australasian relatives (taxa from Australia and New Caledonia) it appears that the family is divided with the most northern New Zealand taxa (tusked weta) more closely related to New Caledonian taxa while all other New Zealand taxa are more closely related to Australian taxa. There does not appear to be any link between the Australian and New Caledonian taxa studied here. Results should be viewed with caution however as an increased mutation rate was observed in the New Caledonian-tusked weta lineage, something future studies will have to address. Chapter Three presents new sequence data and phylogenetic analyses that go towards resolving the apparent basal polytomy of neoavian birds. This chapter includes analyses carried out on previously published data with the addition of nine new mitochondrial genomes. My contribution to this larger project was to perform the phylogenetic analysis and to sequence three of the nine mitochondrial genomes. The genomes I sequenced were the Southern Hemisphere species: dollar bird (Eurystomus orientalis), Owlet nightjar (Aegotheles cristatus cristatus) and great potoo (Nyctibius grandis). The inclusion of these nine new genomes allows assessment and comparison of the six hypothesised groups reported in Cracraft (2001). First an improved conditional down-weighting technique is described reducing noise relative to signal, which is important for resolving deeper divergences. Second, a formula is presented for calculating probabilities of finding predefined groupings in the optimal tree. Maximum likelihood and Bayesian based phylogenetic analyses were carried out and in addition, dating using a relaxed molecular clock was performed in BEAST. Results suggested that the six groups suggested by Cracraft (2001) represent robust lineages. The results suggested that one group, the owls, are more closely related to other raptors, particularly accipitrids (buzzards/eagles) and the osprey rather than the Caprimulgiformes, which could indicate morphological convergent evolution. In addition, a group termed shorebirds appears to be distinct from the large group referred to as ‘Conglomerati’ to which previous publications have suggested they belong. The ‘Conglomerati’ is the least well studied group and may actually comprise of at least three subgroups (as suggested by Cracraft). Within the three suggested groups, Cracraft grouped shorebirds with pigeons and sandgrouse, neither of which (pigeons or sandgrouse) were analysed here. So although the shorebirds are at least close to the ‘Conglomerati’ and may be within that group, their exact position is still not clear. The molecular dating reported here utilised two fossil calibrations (Vegavis and Waimanu), for which there is relatively little dispute as to age or the lineage to which they belong. Calibrations resulting from BEAST analyses suggest that at least 12 distinct lineages were present prior to the K – Pg boundary, a finding supported by previous studies. Robust phylogenies will allow future studies to investigate not only the relationships within Neoaves, but look more closely at the biological and ecological evolution of the group. Chapter Four for the first time investigates whether the phylogenetic relationships within the family Anostostomatidae follow the conventionally accepted order and timing of Gondwanan breakup. Following the initial restults for taxa studied in Australasia (Chapter Two) an attempt to resolve family relationships in a wider spatial (geographic) context was carried out to determine if Australasian taxa are monophyletic when other members of the family are included. Again both maximum likelihood and Bayesian phylogenetic analyses were carried out on both mitochondrial (COI and 12S) and nuclear (18S and 28S) sequences. In this chapter, datasets included samples from across the geographic range of Anostostomatidae (South Africa, Madagascar, South America, Australia, New Caledonia and New Zealand), and two clades were observed, congruent with earlier findings. Sequence divergence within geographic regions was found to be relatively high in the mitochondrial genes (COI and 12S) while low in the nuclear ribosomal RNA genes (18S and 28S) as expected given their relative mutation rates. Under the vicariance paradigm, phylogenetic relationships should follow the order of continental breakup, but this was not found. Further, if dispersal and colonisation were continuous, no geographic substructure is expected, however distinct geographic substructure within clades was consistently observed. This interesting phylogenetic pattern may be a case of convergent evolution or paraphyletic sampling which highlights taxonomic issues of the group. Future studies need to include not only molecular data but information on morphology, ecology and behaviour along with the implementation of biogeographic programs that can test alternative hypotheses (such as dispersal and vicariance) directly. Also, the inclusion of the recently reported fossil from the subfamily Euclydesinae (Martins-Neto 2007) should allow for more accurate date estimates within the family. Taken as a whole the results presented in this thesis suggest that microevolutionary processes are sufficient to explain modern diversity without the need to invoke abiotic events. The three cases investigated here - marine inundation, asteroid impact and continental drift - all appear to have had only a limited effect on the diversity of taxa studied. To reach even stronger conclusions future studies should incorporate different data (for instance nuclear genes, intron position, and genome structure) and use biogeographic software capable of including ecological, morphological and habitat information

Data from: Evolution of a hotspot genus: geographic variation in speciation and extinction rates in Banksia (Proteaceae)

Background: Hotspots of angiosperm species richness and endemism in Mediterranean-climate regions are among the most striking, but least well-understood, geographic patterns of biodiversity. Recent studies have emphasized the importance of rapid diversification within hotspots, compared to non-hotspot regions, as a major contributor to these patterns. We constructed the first near-complete phylogeny of Banksia (Proteaceae) to test whether diversification rates have differed between lineages confined to the southwest Australian hotspot and those found throughout southern, eastern and northern Australia. We then tested for variation in diversification rates among the bioclimatic zones within the southwest hotspot itself. Results: Although Banksia species richness in the southwest is ten times that of the rest of the continent, we find little evidence for more rapid diversification in the southwest, although this result is inconclusive. However, we find firmer support for substantial rate variation within the southwest hotspot, with more rapid diversification in the semi-arid heaths and shrublands, compared to the high-rainfall forests. Most of the Banksia diversity of the southwest appears to be generated in the heaths and shrublands, with a high migration rate out of this zone boosting diversity of the adjacent forest zone. Conclusions: The geographic pattern of diversification in Banksia appears more complex than can be characterized by a simple hotspot vs. non-hotspot comparison, but in general, these findings contrast with the view that the high diversity of Mediterranean hotspots is underpinned by rapid radiations. Steady accumulation of species at unexceptional rates, but over long periods of time, may also have contributed substantially to the great botanical richness of these regions

Family-level relationships among the Australasian marsupial 'herbivores' (Diprotodontia: Koala, wombats, kangaroos and possums)

The marsupial order Diprotodontia includes 10 extant families, which occupy all terrestrial habitats across Australia and New Guinea and have evolved remarkable dietary and locomotory diversity. Despite considerable attention, the interrelations of these families have for the most part remained elusive. In this study, we separately model mitochondrial RNA and protein-coding sequences in addition to nuclear protein-coding sequences to provide near-complete resolution of diprotodontian family-level phylogeny. We show that alternative topologies inferred in some previous studies are likely to be artifactual, resulting from branch-length and compositional biases. Subordinal groupings resolved herein include Vombatiformes (wombats and koala) and Phalangerida, which in turn comprises Petauroidea (petaurid gliders and striped, feathertail, ringtail and honey possums) and a clade whose plesiomorphic members possess blade-like premolars (phalangerid possums, kangaroos and their allies and most likely, pygmy possums). The topology resolved reveals ecological niche structuring among diprotodontians that has likely been maintained for more than 40 million years

Systematics of a small Gehyra (Squamata: Gekkonidae) from the Einasleigh Uplands, Queensland: description of a new range restricted species

The tropical savannah landscapes of Australia's north, though previously overshadowed by the biodiverse rainforests of the Wet Tropics, are themselves now attracting interest for their biological significance and uniqueness. The Einasleigh Uplands region of north-east Queensland is home to a diverse group of mammals and reptiles and was previously recognised for its importance in shaping speciation in birds. Here we add a small saxicoline gecko to a growing list of recently described reptiles that are endemic to this region. Phylogenetic analyses including Gehyra species from the arid zone and the monsoonal tropics reveal that small Gehyra geckos in this area, while closely resembling Gehyra nana from the Top End and Kimberley, form a clade that is geographically isolated and phylogenetically distant from the G. nana complex. Instead, the Einasleigh Uplands taxon is sister to a large, arboreal species within the arid zone clade. It is readily distinguished from all lineages within the G. nana complex, its closest relative G. purpurascens, and all other rock-dwelling species from the arid zone by a combination of its very small body size, few subdigital lamellae, and mid tan to golden dorsal coloration with a pattern of scattered pale ocelli and irregular dark-brown blotches on a stippled background. We therefore describe this taxon as a new Australian species of Gehyra, Gehyra einasleighensis sp. nov., based on a combination of phylogenetic separation, morphological characters and discrete geographic distribution

Diversification of New Zealand weta (Orthoptera: Ensifera: Anostostomatidae) and their relationships in Australasia

New Zealand taxa from the Orthopteran family Anostostomatidae have been shown to consist of three broad groups, Hemiandrus (ground weta), Anisoura/Motuweta (tusked weta) and Hemideina–Deinacrida (tree–giant weta). The family is also present in Australia and New Caledonia, the nearest large land masses to New Zealand. All genera are endemic to their respective countries except Hemiandrus that occurs in New Zealand and Australia. We used nuclear and mitochondrial DNA sequence data to study within genera and among species-level genetic diversity within New Zealand and to examine phylogenetic relationships of taxa in Australasia. We found the Anostostomatidae to be monophyletic within Ensifera, and justifiably distinguished from the Stenopelmatidae among which they were formerly placed. However, the New Zealand Anostostomatidae are not monophyletic with respect to Australian and New Caledonian species in our analyses. Two of the New Zealand groups have closer allies in Australia and one in New Caledonia. We carried out maximum-likelihood and Bayesian analyses to reveal several well supported subgroupings. Our analysis included the most extensive sampling to date of Hemiandrus species and indicate that Australian and New Zealand Hemiandrus are not monophyletic. We used molecular dating approaches to test the plausibility of alternative biogeographic hypotheses for the origin of the New Zealand anostostomatid fauna and found support for divergence of the main clades at, or shortly after, Gondwanan break-up, and dispersal across the Tasman much more recently

FIGURE 5 in Systematics of a small Gehyra (Squamata: Gekkonidae) from the Einasleigh Uplands, Queensland: description of a new range restricted species

FIGURE 5. Gehyra einasleighensis sp. nov. in life. Top: dark patterned adult specimen from 6 km south-east of Petford (CCM5160); bottom: golden patterned adult specimen from vicinity of Cobbold Gorge Village (CCM5144) (photographs—C. C. Moritz). Neither individual was taken as a voucher specimen.Published as part of Bourke, Gayleen, Pratt, Renae C., Vanderduys, Eric & Moritz, Craig, 2017, Systematics of a small Gehyra (Squamata: Gekkonidae) from the Einasleigh Uplands, Queensland: description of a new range restricted species, pp. 85-99 in Zootaxa 4231 (1) on page 92, DOI: 10.11646/zootaxa.4231.1.5, http://zenodo.org/record/29363

Systematics of small Gehyra (Squamata: Gekkonidae) of the southern Kimberley, Western Australia: redescription of G. kimberleyi Börner & Schüttler, 1983 and description of a new restricted range species

Oliver, Paul M., Bourke, Gayleen, Pratt, Renae C., Doughty, Paul, Moritz, Craig (2016): Systematics of small Gehyra (Squamata: Gekkonidae) of the southern Kimberley, Western Australia: redescription of G. kimberleyi Börner & Schüttler, 1983 and description of a new restricted range species. Zootaxa 4107 (1): 49-64, DOI: 10.11646/zootaxa.4107.1.