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The process of speciation remains a fundamental topic in evolutionary biology. Numerous models of speciation have been proposed and they are as diverse and colourful as the scientists who conceived them (Coyne & Orr 2004). One of the more controversial theories has been the ‘stasipatric speciation’ model, proposed by the pioneering and influential cytogeneticist Michael White and his co-workers (White 1968; White et al. 1967). This is one of a number of speciation models whereby chromosomal rearrangements drive the speciation process. The inspiration for the theory of stasipatric speciation came from White’s karyotypic analyses of a group of Australian grasshoppers of the genus Vandiemenella (White et al. 1967) (Fig. 1). It has been exactly three decades since the last scientific publication on this group of grasshoppers, over which time the molecular revolution dramatically altered the landscape of evolutionary genetics. Kawakami and colleagues have successfully resurrected the Vandiemenella system (Kawakami et al. 2009a, 2007) and in this issue they have applied modern molecular-based techniques to reassess the validity of the stasipatric speciation model for this historically important group (Kawakami et al. 2009b).
Figure 1. The grasshopper (Vandiemenella viatica) that inspired Michael White to develop the stasipatric speciation model (photograph by Remko Leijs).
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The essential element of the stasipatric model of speciation is that it proceeds by the emergence, fixation and spread of chromosomal rearrangements within a species whose geographic range remains largely in ‘stasis’. It differs from allopatric and sympatric speciation models in that, while populations of the incipient species do not overlap in space, they remain contiguous (at least, with respect to the degree of connectivity among populations that would normally be found across the species’ range). White proposed the stasipatric speciation model to account for numerous cases in which fixed chromosomal rearrangements were associated with recent cases of speciation in organisms of low vagility. White’s good friend Ernst Mayr considered such rearrangements as simply a postspeciation afterthought but White argued that: ‘If this were so, we would expect to frequently encounter the situation where a ‘young’ species or semispecies had different karyotypes in different parts of its range, without these being associated with any genetic isolation (and this is definitely not the case)’ (White 1978, p. 174). This prompted White to consider whether the rearrangements themselves had acted as the isolating mechanism.
Stasipatric speciation sensu stricto would leave none of the classic signatures of population fragmentation that are now routinely studied by phylogeographic methods. Moreover, the genetic structuring should be very strongly associated with the karyotypically defined lineages. Kawakami et al. (2009b) tested the validity of these two criteria in Vandiemenella by applying modern phylogenetic and population genetic analyses to data they collected on karyotypic, allozymic, mitochondrial and nuclear markers. These analyses reveal some evidence for allopatric fragmentation within Vandiemenella, especially in the putatively ancestral karyotypic lineage. Phylogeographic breaks are also revealed, that correspond with potential geographic barriers but not with the karyotypic taxa. The most significant of these is associated with the Murray River and potentially the ancient Lake Bungunnia (Bowler et al. 2006) (Fig. 2). The effect of this barrier is seen most strikingly in the phylogeny for an anonymous nuclear marker Mvia11, which divides the entire lineage into two broad clades. We suggest that active dune-fields during recent glacial maxima may also have had an isolating influence (Fig. 2). Moreover, the Murray River may not be a strong barrier to morabine grasshoppers in general, with a recently evolved parthenogenetic species also studied by White having clearly spread across it (Kearney et al. 2006). Kawakami et al. (2009b) do not speculate on the timing of events in Vandiemenella; but if, as they suggest, Lake Bungunnia was responsible for this fragmentation, it likely happened between 0.7 and 2.5 Ma.
With respect to genetic structuring, much (40–65%) of the nuclear genetic variation is captured by the chromosomal rearrangements deciphered by White and colleagues, yet there is also strong evidence for a degree of mixing or introgression among many lineages. This is particularly rampant for the mitochondrial genome, which has passed with almost no restriction among chromosomal taxa. Thus, some karyotypic taxa are spread across multiple genetically defined groups, and vice versa (e.g. Fig. 2). In fact, the level of introgression is so high that it led Kawakami et al. (2009b) to concur with Key (1968) in denying species-level status for all but one of the 11 previously defined karyotypic taxa. Hence the group may approach White’s antithetical case quoted above of a karyotypically differentiated young species with some level of gene flow between lineages.
The stasipatric model of speciation in Vandiemenella was criticized by previous authors, one of us included (Futuyma & Mayer 1980; Hewitt 1979; Key 1968). Major criticisms centred on the difficulty of chromosomal mutants reaching fixation (White invoked meiotic drive) and the plausibility of simpler, allopatric models. The observations of Kawakami et al. (2009b) are inconsistent with the stasipatric speciation model sensu stricto, but do they completely bury it? Perhaps not, as recent theoretical work shows that chromosomal inversions may be favoured because they suppress recombination in some regions, allowing locally adapted mutations to accumulate in the face of maladapted gene flow (Kirkpatrick & Barton 2006). This process is not limited to coadapted alleles, as in some previous models, and thus may provide a very general and powerful selective agent favouring certain chromosomal rearrangements. Thus it is still possible that chromosomal changes have had a causal role in the diversification of the Vandiemenella group, albeit in a somewhat different way to that envisaged by White.
Both Key (1968) and Hewitt (1979) thought that peripheral allopatric origins of the chromosomal rearrangement races as more likely than stasipatry. Hewitt (1979) considered the Flinders Ranges and coast of the Eyre Peninsula (Fig. 2) during glacial periods as most likely areas for the origins of new chromosomal taxa. The last three decades have also seen considerable advances in our thinking about the effects of Pleistocene climatic oscillations on genetic divergence and speciation (Hewitt 2004), so that repeated contractions and expansions of Vandiemenella’s habitat and range seem important factors in the evolution of its complex genetic structure. Kawakami et al. (2009b) consider it likely that allopatric fragmentation produced by such processes has played a significant role in the diversification of Vandiemenella’s genome. In particular, the widely distributed ‘viatica 19’ karyotype is shown to comprise several clearly diverged genomes, some disjunct, probably ancient and likely refugial, as in the case of the population from Tasmania (Fig. 2). The region towards the northwest of the range, including the gulfs and peninsulas between the Flinders Ranges and Kangaroo Island, is notable in containing a complex patchwork of chromosome and genomic races; it seems likely that the topography, sea level changes, dune formation and habitat shifts through climatic oscillations in this region were causal in generating such genetic patterns of divergence, as recently indicated in other parts of the world.
In resurrecting the Vandiemenella system and applying modern approaches, Kawakami et al. (2009b) have provided a novel perspective on an important system in speciation theory. This system will undoubtedly continue to provide us with new insights into the speciation process. It is truly unfortunate that we cannot obtain the perspectives of Michael White and Ken Key on the findings of Kawakami et al. (2009b). It is tempting to imagine their responses. Ken Key was a deep-thinking scientist, and would have been pleased that his use of ‘P’ provisional taxonomic designations had been vindicated, when others were pushing for specific status for such karyotypic divergence. On the other hand, Michael White would have thrown himself into experimental research to test and clarify the system further, as he did for his Warramaba virgo group when new hypotheses were suggested. White tended to dismiss mating behaviour as a major factor in Morabine speciation—‘they are rather primitive’—and the hybridization between deeply diverged taxa would support this view. In this respect, the group may resemble some frogs, where speciation seems to take a long time. But the role of mating behaviour of Vandiemenella in this process deserves study, and White would probably have had a go.