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Chromosomal Speciation in the Genomics Era: Disentangling Phylogenetic Evolution of Rock-wallabies - PubMed

  • ️Sun Jan 01 2017

Chromosomal Speciation in the Genomics Era: Disentangling Phylogenetic Evolution of Rock-wallabies

Sally Potter et al. Front Genet. 2017.

Abstract

The association of chromosome rearrangements (CRs) with speciation is well established, and there is a long history of theory and evidence relating to "chromosomal speciation." Genomic sequencing has the potential to provide new insights into how reorganization of genome structure promotes divergence, and in model systems has demonstrated reduced gene flow in rearranged segments. However, there are limits to what we can understand from a small number of model systems, which each only tell us about one episode of chromosomal speciation. Progressing from patterns of association between chromosome (and genic) change, to understanding processes of speciation requires both comparative studies across diverse systems and integration of genome-scale sequence comparisons with other lines of evidence. Here, we showcase a promising example of chromosomal speciation in a non-model organism, the endemic Australian marsupial genus Petrogale. We present initial phylogenetic results from exon-capture that resolve a history of divergence associated with extensive and repeated CRs. Yet it remains challenging to disentangle gene tree heterogeneity caused by recent divergence and gene flow in this and other such recent radiations. We outline a way forward for better integration of comparative genomic sequence data with evidence from molecular cytogenetics, and analyses of shifts in the recombination landscape and potential disruption of meiotic segregation and epigenetic programming. In all likelihood, CRs impact multiple cellular processes and these effects need to be considered together, along with effects of genic divergence. Understanding the effects of CRs together with genic divergence will require development of more integrative theory and inference methods. Together, new data and analysis tools will combine to shed light on long standing questions of how chromosome and genic divergence promote speciation.

Keywords: chromosome rearrangement; divergence; genomics; rock-wallaby; speciation.

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Figures

FIGURE 1
FIGURE 1

Map of rock-wallaby (Petrogale) taxa distributions across Australia. Map modified from Eldridge and Close (1993). Taxa are colored in accordance with their chromosomal groupings: the brachyotis group = red; the xanthopus group = yellow; the lateralis group = blue; and the penicillata group = green.

FIGURE 2
FIGURE 2

(A) Phylogenetic relationships of rock-wallabies (Petrogale) based on a maximum likelihood analysis of concatenated nuclear data (1961 loci). Bootstrap support < 100% is outlined on the nodes, ∗ = < 50%; nodes with neither have support of 100%. Four chromosomal groups are highlighted on the phylogeny: the brachyotis group = red; the xanthopus group = yellow; the lateralis group = blue; and the penicillata group = green. Karyotype variation (2n) for each of the four chromosomal groups is highlighted. Dendrolagus lumholtzi (tree kangaroo) and Thylogale thetis (pademelon) are used as outgroups. (B) A maximum likelihood mitochondrial phylogeny of Petrogale based on all mitochondrial coding genes (12 loci). Chromosomal groups are highlighted to match (A), as is bootstrap support.

FIGURE 3
FIGURE 3

Reconstruction of chromosomal rearrangements based on parsimony analysis for Petrogale using only known chromosomal karyotypes (e.g., no sub-species for P. brachyotis, P. concinna or P. xanthopus). Reconstructions of ancestral karyotypes are highlighted on the main phylogeny and those that could not be resolved for nodes in the phylogeny are indicated in blue for chromosomes 3, 4, and 5. See Supplementary Table 2 for character state matrix. Chromosomal groups are again outlined in color: brachyotis = red; xanthopus = yellow; lateralis = blue; and penicillata = green. Chromosomal rearrangements include: centric shifts, a = acrocentric, m = metacentric, sm = submetacentric; inversions (i); and fusions between two chromosomes (-).

FIGURE 4
FIGURE 4

Graph of average net divergence between taxa within each chromosomal group: brachyotis, lateralis, penicillata, and xanthopus. Divergences are estimated for loci on the X chromosome, non-rearranged chromosomes (2,4,7,8) and rearranged chromosomes (5,6,9,10).

FIGURE 5
FIGURE 5

Maximum likelihood phylogenies of Petrogale taxa based on loci from the X chromosome, rearranged autosomal chromosomes (5,6,9,10) and non-rearranged autosomal chromosomes (2,4,7,8). Bootstrap support is highlighted on the nodes of the tree. Incongruence in the phylogenetic reconstruction to the concatenated nuclear phylogeny (Figure 2A) is highlighted in red on each tree.

FIGURE 6
FIGURE 6

(A–C) A phylogenetic network analysis of the chromosomal groups (A) brachyotis, (B) lateralis, and (C) penicillata estimated using a distance based approach in SplitsTree (Neighbor-Net). The red arrows highlight regions on the network where reticulation is inferred. (D–F) Model based analysis of reticulate evolutionary history based on analysis of 0–3 reticulations. The lowest log likelihood results are shown for each (D) brachyotis, (E) lateralis, and (F) penicillata chromosomal groups using PhyloNet. Analysis was performed on a single individual for each taxon and two replicate analyses, each including one of the two independent samples per taxon. (D) The brachyotis group supported 2–3 reticulations and highlight reticulation involving ancestors in the brachyotis group. (E) The penicillata group analysis include a three species complex (P. assimilis, P. mareeba, and P. sharmani) and support a single reticulation model but alternate topologies and individuals involved in reticulation based on the individuals used in the analysis. (F) The lateralis group analyses included three taxa (P. l. lateralis, P. l. hacketti and P. l. West Kimberley race). The results were congruent in identifying a single reticulation model, which involved the P. lateralis West Kimberley race.

FIGURE 7
FIGURE 7

A schematic overview of an integrative approach to increase understanding how chromosomal rearrangements create divergence and speciation. The hierarchy outlined progresses from simple to complex and may not be feasible for all non-model systems, but outlines the ultimate goals. Blue boxes highlight the processes, yellow boxes highlight the analyses and red boxes highlight the data needed to achieve a holistic understanding of chromosomal speciation. CR, chromosome rearrangement; HQ, high quality.

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