Evolutionary Pace of Chromosomal Polymorphism in Colonizing Populations of Drosophila Subobscura: An Evolutionary Time Series

Abstract

Biologists have long debated the speed, uniformity, and predictability of evolutionary change. However, evaluating such patterns on a geographic scale requires time-series data on replicate sets of natural populations. Drosophila subobscura has proven an ideal model system for such studies. This fly is broadly distributed in the Old World, but was introduced into both North and South America just over two decades ago and then spread rapidly. Rapid, uniform, and predictable evolution would be demonstrated if the invading flies evolved latitudinal clines that progressively converged on those of the native populations. Evolutionary geneticists quickly capitalized on this opportunity to monitor evolutionary dynamics. Just a few years after the introduction, they surveyed chromosomal inversion frequencies in both North and South America. On both continents they detected incipient latitudinal clines in chromosome inversion frequencies that almost always had the same sign with latitude as in the Old World. Thus the initial evolution of chromosomal polymorphisms on a continental scale was remarkably rapid and consistent. Here we report newer samples of inversion frequencies for the colonizing populations: the time series now spans almost one decade for North America and almost two decades for South America. Almost all inversions in the New World continue to show the same sign of frequency with latitude as in the Old World. Nevertheless, inversion clines have not consistently increased in steepness over time; nor have they consistently continued to converge on the Old World baseline. However, five arrangements in South America show directional, continentwide shifts in frequency. Overall, the initial consistency of clinal evolutionary trajectories seen in the first surveys seems not to have been maintained.

Thermal evolution of gene expression profiles in Drosophila subobscura

“…The data also suggest an association with polymorphic inversions as some clustering of genes within inverted chromosomal sections was detected. This result is probably not surprising in view of the rapidly evolved latitudinal clines in inversion frequencies after the introduction of the species into the New World [12], as well as the quick response of inversion polymorphism to laboratory temperature [16]. The challenge now is to elucidate what associations are causal and what are due to correlated responses or hitchhiking arisen from linkage disequilibrium with the inversions.…”

“…Remarkably enough, latitudinal clines in the New World for inversion polymorphism and body size parallel to the long standing ones in the native geographic area were evident after a few years since the American colonization. This 'replicated time series experiment of evolution in action' [12,13] strongly suggests that those traits are indeed subject to selection from temperature-related factors. However, a laboratory natural selection experiment (i.e., an experimental protocol where stocks of organisms are reared under different conditions and allowed to evolve by natural selection over many generations [14]) specifically designed to test the putative role of temperature per se in the evolution of these clines found results conflicting to those expected from the latitudinal gradients for both inversions and body size [3,15,16].…”

“…[31,32]), and quantitative associations between larval gene expression and thermal adaptation could be due to position effects (e.g., the inversion of a chromosomal segment can remove or exchange the regulatory sequences of a gene and alter its expression pattern [33]) or hitchhiking arisen from linkage disequilibrium. In view of the rapidly and consistently evolved latitudinal clines in chromosome inversion polymorphism following the New World invasion by the species [12], and the shifts in inversion frequencies in response to laboratory thermal adaptation [16] and to climate change [7], we expect that a large number of genes will be included inside inverted chromosome segments. Linkage with inversions will highly complicate the identification of chromosome regions that are targets of selection.…”

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“…In colonizing populations of the New World only six gene arrangements are segregating for that chromosome: O st , O 3+4 , O 3+4+2 , O 3+4+7 , O 3+4+8 and O 5 (arrangement O 7 is also present at very low frequency but it is probably the result of a recombination event in the O st /O 3+4+7 heterokaryotype [35]). In native Palearctic populations arrangements O 3+4+2 and O 3+4+8 are restricted to the Mediterranean region (the likely area from which the original American colonists derived [36]) and are not involved in latitudinal clines [35]. On the other hand, arrangement O st shows a world-wide positive correlation with latitude, while arrangements O 3+4 and O 3+4+7 show a contrasting pattern [35].…”

“…In native Palearctic populations arrangements O 3+4+2 and O 3+4+8 are restricted to the Mediterranean region (the likely area from which the original American colonists derived [36]) and are not involved in latitudinal clines [35]. On the other hand, arrangement O st shows a world-wide positive correlation with latitude, while arrangements O 3+4 and O 3+4+7 show a contrasting pattern [35]. Therefore, six independent isochromosomal lines for each of these three chromosome arrangements (i.e., , ..., ; j = st, 3+4, 3+4+7) were used in the present experiments.…”