Abstract
Chromosomal rearrangements can alter the rate and patterns of gene flow within or between species through a reduction in the fitness of chromosomal hybrids or by reducing recombination rates in rearranged areas of the genome. This concept, together with the observation that many species have structural variation in chromosomes, has led to the theory that the rearrangements may play a direct role in promoting speciation. Australian morabine grasshoppers (genus Vandiemenella, viatica species group) are an excellent model for studying the role of chromosomal rearrangement in speciation because they show extensive chromosomal variation, parapatric distribution patterns, and narrow hybrid zones at their boundaries. This species group stimulated development of one of the classic chromosomal speciation models, the stasipatric speciation model proposed by White in 1968. Our population genetic and phylogeographic analyses revealed extensive non-monophyly of chromosomal races along with historical and on-going gene introgression between them. These findings suggest that geographical isolation leading to the fixation of chromosomal variants in different geographic regions, followed by secondary contact, resulted in the present day parapatric distributions of chromosomal races. The significance of chromosomal rearrangements in the diversification of the viatica species group can be explored by comparing patterns of genetic differentiation between rearranged and co-linear parts of the genome.
Highlights
Speciation is the evolutionary process that leads to barriers to gene exchange between taxa, and understanding the factors that give rise to such barriers is a central theme of evolutionary biology [1].Variation in the structure of chromosomes has long been considered to provide barriers to gene flow between hybridizing taxa with different karyotypes; whether such changes play a direct role in the process of speciation has been much debated [2,3,4]
Certain types of chromosomal rearrangements have the opportunity to be actively involved in speciation processes by reducing fertility of chromosomal heterozygotes, many of the traditional chromosomal speciation models suffer from critical theoretical problems
How does chromosomal divergence correlate with genetic divergence? Are chromosomal variants in the group associated with barriers to gene flow? Is there any evidence for an allopatric phase during diversification of the group, or have chromosomal races diversified without geographic isolation as the stasipatric model predicts? To provide new insights into these questions, we have explored the population genetic structure and phylogeography of the group across their range in southeastern Australia and investigated the level of introgression of molecular genetic markers among the chromosomal taxa using a combination of allozymes, microsatellites, two nuclear DNA sequences (Elongation Factor 1α [EF-1α] and an anonymous nuclear marker Mvia11)
Summary
Speciation is the evolutionary process that leads to barriers to gene exchange between taxa, and understanding the factors that give rise to such barriers is a central theme of evolutionary biology [1]. Based on these studies in the viatica species group, White argued that chromosomal changes play a causative role in speciation by leading to hybrid dysfunction or underdominance of heterokaryotypic individuals and proposed a classic chromosomal speciation model, called the ‘stasipatric speciation model’ [2,28] Key features of this model include (i) chromosomal rearrangements produce barriers to gene flow between parental and daughter chromosome types due to meiotic abnormalities in chromosomal heterozygotes, and (ii) the spread of new chromosome types from their point of origin into the distribution of a parental chromosome type occurs without geographic isolation, leading to parapatric distributions of chromosomal races. We highlight that this classic study system provides an unprecedented opportunity to explore the new chromosomal speciation theories
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