Gillian C. Gibb

Mutation and Evolutionary Rates in Adélie Penguins from the Antarctic

Precise estimations of molecular rates are fundamental to our understanding of the processes of evolution. In principle, mutation and evolutionary rates for neutral regions of the same species are expected to be equal. However, a number of recent studies have shown that mutation rates estimated from pedigree material are much faster than evolutionary rates measured over longer time periods. To resolve this apparent contradiction, we have examined the hypervariable region (HVR I) of the mitochondrial genome using families of Adélie penguins (Pygoscelis adeliae) from the Antarctic. We sequenced 344 bps of the HVR I from penguins comprising 508 families with 915 chicks, together with both their parents. All of the 62 germline heteroplasmies that we detected in mothers were also detected in their offspring, consistent with maternal inheritance. These data give an estimated mutation rate (μ) of 0.55 mutations/site/Myrs (HPD 95% confidence interval of 0.29–0.88 mutations/site/Myrs) after accounting for the persistence of these heteroplasmies and the sensitivity of current detection methods. In comparison, the rate of evolution (k) of the same HVR I region, determined using DNA sequences from 162 known age sub-fossil bones spanning a 37,000-year period, was 0.86 substitutions/site/Myrs (HPD 95% confidence interval of 0.53 and 1.17). Importantly, the latter rate is not statistically different from our estimate of the mutation rate. These results are in contrast to the view that molecular rates are time dependent.

Tinamous and Moa Flock Together: Mitochondrial Genome Sequence Analysis Reveals Independent Losses of Flight among Ratites

Ratites are large, flightless birds and include the ostrich, rheas, kiwi, emu, and cassowaries, along with extinct members, such as moa and elephant birds. Previous phylogenetic analyses of complete mitochondrial genome sequences have reinforced the traditional belief that ratites are monophyletic and tinamous are their sister group. However, in these studies ratite monophyly was enforced in the analyses that modeled rate heterogeneity among variable sites. Relaxing this topological constraint results in strong support for the tinamous (which fly) nesting within ratites. Furthermore, upon reducing base compositional bias and partitioning models of sequence evolution among protein codon positions and RNA structures, the tinamou-moa clade grouped with kiwi, emu, and cassowaries to the exclusion of the successively more divergent rheas and ostrich. These relationships are consistent with recent results from a large nuclear data set, whereas our strongly supported finding of a tinamou-moa grouping further resolves palaeognath phylogeny. We infer flight to have been lost among ratites multiple times in temporally close association with the Cretaceous-Tertiary extinction event. This circumvents requirements for transient microcontinents and island chains to explain discordance between ratite phylogeny and patterns of continental breakup. Ostriches may have dispersed to Africa from Eurasia, putting in question the status of ratites as an iconic Gondwanan relict taxon.

Molecular Phylogeny, Biogeography, and Habitat Preference Evolution of Marsupials

Marsupials exhibit great diversity in ecology and morphology. However, compared with their sister group, the placental mammals, our understanding of many aspects of marsupial evolution remains limited. We use 101 mitochondrial genomes and data from 26 nuclear loci to reconstruct a dated phylogeny including 97% of extant genera and 58% of modern marsupial species. This tree allows us to analyze the evolution of habitat preference and geographic distributions of marsupial species through time. We found a pattern of mesic-adapted lineages evolving to use more arid and open habitats, which is broadly consistent with regional climate and environmental change. However, contrary to the general trend, several lineages subsequently appear to have reverted from drier to more mesic habitats. Biogeographic reconstructions suggest that current views on the connectivity between Australia and New Guinea/Wallacea during the Miocene and Pliocene need to be revised. The antiquity of several endemic New Guinean clades strongly suggests a substantially older period of connection stretching back to the Middle Miocene and implies that New Guinea was colonized by multiple clades almost immediately after its principal formation.

Two aspects along the continuum of pigeon evolution: A South-Pacific radiation and the relationship of pigeons within Neoaves

Phylogenetics explores the continuum of shallower to deeper genetic divergences between taxa. Along this continuum increasing lengths of DNA sequence can be used to answer deeper and deeper questions about biological relationships. We use shorter, and then longer mitochondrial DNA sequences to address two aspects of pigeon evolution. Firstly, we examine the phylogenetic relationships of the eight genera within the South Pacific Ducula-Ptilinopus radiation, and examine how this radiation fits into pigeons generally. Within Ducula, taxa are closely related, whereas Ptilinopus is very diverse, and paraphyletic. One third of all pigeon species are within the Ducula-Ptilinopus radiation, however all are very similar ecologically. Secondly, we study the deeper phylogenetic question regarding the relationship of pigeons to other birds. To this end, we report the complete mitochondrial genome of Hemiphaganovaeseelandiae, a member of the Ducula-Ptilinopus radiation. We use this mitochondrial genome, along with additional sandgrouse (Pterocles namaqua) mitochondrial genes to assess various candidates for the closest relative of pigeons. Of parrots, shorebirds, and sandgrouse, we find highest support for the sandgrouse-pigeon grouping. Furthermore in these analyses the pigeon and sandgrouse group closer to the falcons than any other included taxon. The finding that pigeons and sandgrouse may be more closely related to falcons than to previous candidates such as shorebirds or parrots invites further investigation.

Deep global evolutionary radiation in birds: diversification and trait evolution in the cosmopolitan bird family Rallidae.

Sufficient breadth of taxon sampling in major organisms groups is important to identify more realistic biological diversification processes that reveal the degree of historical biogeographic signal and net diversification retained in the current lineage distribution. We examine the mechanisms driving diversity in one of the major avian clades with an exceptional large-scale radiation, the family Rallidae, using the most complete species-level (∼70%) time calibrated hypothesis of evolutionary relationships produced to date. We find that Rallidae exhibit a pattern of diversification involving episodes of range expansion and regional speciation that results in most clades represented in all habitable continents. Our results suggest that several features may have played an important role on the diversification rates in Rallidae. Lineage accumulation is nearly constant and morphology (frontal shield and body size), innovate (flightlessness), habitat (forest) and distribution (insular) traits are possibly associated with increasing diversification rates along with spatial and ecological processes during the Miocene and Pliocene. Diversification and the global retention of lineage diversity have occurred in multiple lineages in Rallidae due to their dispersal ability and exploitation of ecological opportunities.

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.

New Zealand Passerines Help Clarify the Diversification of Major Songbird Lineages during the Oligocene

Abstract Passerines are the largest avian order, and the 6,000 species comprise more than half of all extant bird species. This successful radiation probably had its origin in the Australasian region, but dating this origin has been difficult due to a scarce fossil record and poor biogeographic assumptions. Many of New Zealand’s endemic passerines fall within the deeper branches of the passerine radiation, and a well resolved phylogeny for the modern New Zealand element in the deeper branches of the oscine lineage will help us understand both oscine and passerine biogeography. To this end we present complete mitochondrial genomes representing all families of New Zealand passerines in a phylogenetic framework of over 100 passerine species. Dating analyses of this robust phylogeny suggest Passeriformes originated in the early Paleocene, with the major lineages of oscines “escaping” from Australasia about 30 Ma, and radiating throughout the world during the Oligocene. This independently derived conclusion is consistent with the passerine fossil record.

Phylogenetic Position of Avian Nocturnal and Diurnal Raptors

We report three new avian mitochondrial genomes, two from widely separated groups of owls and a falcon relative (the Secretarybird). We then report additional progress in resolving Neoavian relationships in that the two groups of owls do come together (it is not just long-branch attraction), and the Secretarybird is the deepest divergence on the Accipitridae lineage. This is now agreed between mitochondrial and nuclear sequences. There is no evidence for the monophyly of the combined three groups of raptors (owls, eagles, and falcons), and again this is agreed by nuclear and mitochondrial sequences. All three groups (owls, accipitrids [eagles], and falcons) do appear to be members of the “higher land birds,” and though there may not yet be full “consilience” between mitochondrial and nuclear sequences for the precise order of divergences of the eagles, falcons, and the owls, there is good progress on their relationships.

Intergenerational mutation rate does not equal long-term evolutionary substitution rate

Recently in PNAS, Langergraber et al. (1) presented interesting findings regarding body size and generation times in chimpanzees and gorillas. The authors then combined these data with recent whole-genome estimates of human mutation rate per generation to recalibrate previous estimates of divergence times in great apes and humans. The authors’ divergence estimates are older than previous findings, which reduce the conflict of previous estimates with some contentious older fossil hominins. It is important to have accurate estimations of generation time, but the authors were quick to apply new intergenerational mutation rates to estimates of divergences millions of years ago, without consideration of the issues this has raised in the past (see ref. 2).

The complete mitochondrial genome of the eastern grey kangaroo (Macropus giganteus)

Abstract We present the complete mitochondrial genome (accession number: LK995454) of an iconic Australian species, the eastern grey kangaroo (Macropus giganteus). The mitogenomic organization is consistent with other marsupials, encoding 13 protein-coding genes, 22 tRNA genes, 2 ribosomal RNA genes, an origin of light strand replication and a control region or D-loop. No repetitive sequences were detected in the control region. The M. giganteus mitogenome exemplifies a combination of tRNA gene order and structural peculiarities that appear to be unique to marsupials. We present a maximum likelihood phylogeny based on complete mitochondrial protein and RNA coding sequences that confirms the phylogenetic position of the grey kangaroo among macropodids.