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.
Highlights
Differences in how the genome is packaged – chromosome variation – have long been known to influence how genetic variation is transmitted and redistributed within and among populations (Darlington, 1958; White, 1973)
We highlight a case study that emphasizes how a combined knowledge of genome architecture and genomic sequence divergence is important for understanding the history of chromosomal rearrangements (CRs) in association with speciation and being able to assess whether gene flow is reduced in rearranged regions
The results suggested reticulation amongst P. coenensis and P. godmani, between P. assimilis, P. mareeba and P. sharmani, as well as between P. lateralis lateralis and P. lateralis West Kimberley race (Figure 6)
Summary
Differences in how the genome is packaged – chromosome variation – have long been known to influence how genetic variation is transmitted and redistributed within and among populations (Darlington, 1958; White, 1973). It has been highlighted that introgression, retained ancestral polymorphism (or ILS) has resulted in paraphyletic species complexes within both the brachyotis group (see Potter et al, 2012a,b) and the penicillata group (Briscoe et al, 1982; Bee and Close, 1993; Potter et al, 2015) This is the first analysis using all coding genes across the mitochondrial genome, providing the most phylogenetic information and highlight discrepancies to the nuclear phylogeny, in particular – the placement of P. persephone and P. xanthopus as basal branches; the paraphyly of brachyotis group taxa; and lack of monophyly for P. assimilis, P. coenensis and P. godmani within the penicillata group. The key here will be finding systems where CRs are relatively recent, to distinguish between genic divergence post speciation vs. mutations causing reproductive isolation in relation to genomic architecture
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