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.