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doi: 10.1371/journal.pone.0057745. Epub 2013 Feb 22.

Inferring kangaroo phylogeny from incongruent nuclear and mitochondrial genes

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Inferring kangaroo phylogeny from incongruent nuclear and mitochondrial genes

Matthew J Phillips et al. PLoS One.2013.

Abstract

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.

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Conflict of interest statement

Competing Interests:The authors have declared that no competing interests exist.

Figures

Figure 1
Figure 1. Phylogenetic relationships ofWallabia and the threeMacropus subgenera,M. (Macropus),M. (Osphranter) andM. (Notamacropus).
(A) The supertree of Cardillo et al. summarizing previous molecular and morphological phylogenies and (B) Meredith et al.'s evolutionary timescale (ave. of four BEAST analyses), showing the 2–2.4 Ma duration divergence cluster. Both trees are modified to include only the taxa sampled in the present study. Dendrolagini was not recovered by Cardillo et al. , however its inclusion in the summary tree is warranted on subsequent strong evidence from morphology and all recent molecular analyses. Photos include (from the top)W. bicolor,M. rufogriseus (left),M. irma (right),M. rufus and M. giganteus. Photo credits – Matt Phillips, exceptM. irma (Ric Dawson) andM. rufus (Daniel Hoops).
Figure 2
Figure 2. Phylogenetic analysis of kangaroos and wallabies.
Maximum likelihood phylogenies inferred from the (A) mitochondrial (Mt16) and (B) nuclear (Nuc17) concatenated datasets, with RAxML bootstrap values (BPML) above branches and MrBayes Bayesian posterior probabilities (BPP) below branches. The mt placement ofM. dorsalis is derived from the reduced-length Mt17 and the mt placements ofM. antilopinus andW. bicolor (NSW, New South Wales) are derived from theCytb18 alignment. Support for groupingM. eugenii andM. agilis increases (BPML = 88; BPP = 0.98) for Mt16, which excludesM. dorsalis, but increases sequence length. Asterisks indicate full support. Clades including members ofMacropus are shaded.
Figure 3
Figure 3. Macropodid clade support from datasets simulated under coalescence.
(A) Simulation workflow. (B) Mean number of the five nuclear genes supporting each clade in maximum likelihood analyses of 200 simulations of the combined data *BEAST species tree forNe values of 1,000 (triangle), 10,000 (open circle), 100,000 (square) and 1,000,000 (filled circle). For comparison, the grey bars show the number of genes supporting each clade on the observed data. (C) Percentage of ML analyses supporting each clade among 200 mtDNA simulations on the nuclear-only *BEAST species tree forNe values set to mitochondrial equivalency for the same populations (one quarter of the corresponding nuclear values). Abbreviations:Lagor.;Lagorchestes,Wall.;Wallabia,M. (Notamac.);M. (Notamacropus),M. (Osphran.);M. (Osphranter).
Figure 4
Figure 4. Macropodid species tree estimates from the combined mitochondrial and nuclear sequences (MtNuc16).
(A) concatenated sequences, showing BPP/BPML (@ = 0.89/59), (B) *BEAST partitioned between the mtDNA and five nuclear genes, showing BPP values. (C) both MDC and BUCKy, which recovered the same tree from the mt and five nuclear gene trees. (D) Meredith et al. (2008) with BPML values included for comparison. Several supraspecific clades that were identical across all reconstructions were collapsed for visualization convenience. Relationships within each of the collapsed clades were as inferred in Figure 2. Asterisks indicate full BPP or BPML support.
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This work has been supported by Australian Research Council grants to MJP (DP07745015) and MB (FT0991741). The website for the funder iswww.arc.gov.au. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

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