Luis Serra

Global Genetic Change Tracks Global Climate Warming in Drosophila subobscura

Comparisons of recent with historical samples of chromosome inversion frequencies provide opportunities to determine whether genetic change is tracking climate change in natural populations. We determined the magnitude and direction of shifts over time (24 years between samples on average) in chromosome inversion frequencies and in ambient temperature for populations of the fly Drosophila subobscura on three continents. In 22 of 26 populations, climates warmed over the intervals, and genotypes characteristic of low latitudes (warm climates) increased in frequency in 21 of those 22 populations. Thus, genetic change in this fly is tracking climate warming and is doing so globally.

A time series of evolution in action: a latitudinal cline in wing size in South American Drosophila subobscura.

Abstract Drosophila subobscura is geographically widespread in the Old World. Around the late 1970s, it was accidentally introduced into both South and North America, where it spread rapidly over broad latitudinal ranges. This invading species offers opportunities to study the speed and predictability of trait evolution on a geographic scale. One trait of special interest is body size, which shows a strong and positive latitudinal cline in many Drosophila species, including Old World D. subobscura. Surveys made about a decade after the invasion found no evidence of a size cline in either North or South America. However, a survey made in North America about two decades after the invasion showed that a conspicuous size cline had evolved and (for females) was coincident with that for Old World flies. We have now conducted parallel studies on 10 populations (13° of latitude) of flies, collected in Chile in spring 1999. After rearing flies in the laboratory for several generations, we measured wing sizes and compared geographic patterns (versus latitude or temperature) for flies on all three continents. South American females have now evolved a significant latitudinal size cline that is similar in slope to that of Old World and of North American flies. Rates of evolution (haldanes) for females are among the highest ever measured for quantitative traits. In contrast, the size cline is positive but not significant for South or North American males. At any given latitude, South American flies of both sexes are relatively large; this in part reflects the relatively cool climate of coastal Chile. Interestingly, the sections of the wing that generate the size cline for females differ among all three continents. Thus, although the evolution of overall wing size is predictable on a geographic scale (at least for females), the evolution of size of particular wing components is decidedly not.

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.

THE COLONIZATION OF DROSOPHILA SUBOBSCURA IN CHILE. II. CLINES IN THE CHROMOSOMAL ARRANGEMENTS

Drosophila subobscura is a Palearctic species that was first detected in the New World in Puerto Montt (Chile) in February 1978. Since that time, it has spread over a broad area and increased in population density. The South American populations exhibit a high level of chromosomal polymorphism: 20 different arrangements exist, distributed among five chromosomes. Chromosomal arrangement heterozygosity varies from 0.55 to 0.61 in the nine populations examined. Incipient clines in the frequencies of the arrangements are appearing; these clines follow the same latitudinal direction as in the Old World. Wing length significantly decreases with latitude, as it does in Europe. The colonization of South America by D. subobscura appears to be a major natural experiment with outcomes that duplicate the distributional patterns—in chromosomal polymorphism and in wing length—observed in the Old World, thereby strongly supporting the adaptive significance of these patterns. The data show a very rapid effect of natural selection promoting genetic differentiation among natural populations.

LONG-TERM CHANGES IN THE CHROMOSOMAL INVERSION POLYMORPHISM OF DROSOPHILA SUBOBSCURA. I. MEDITERRANEAN POPULATIONS FROM SOUTHWESTERN EUROPE

Abstract The chromosomal polymorphism of seven Mediterranean populations of Drosophila subobscura has been compared with that of the same populations collected 26 to 35 years ago. Significant latitudinal clines for the frequencies of AST, EST, OST, and UST chromosomal arrangements have been detected in the old and new samples. Standard gene arrangements are frequent in the north and decrease in frequency towards the south. Significant negative regression coefficients between latitude and transformed frequency have also been observed for the more frequent nonstandard gene arrangements. The pattern of the clines is practically the same in the old and new collections. Furthermore, the frequencies of gene arrangements of all chromosomes have changed significantly during this period in a systematic way: an increase in the frequency of those arrangements typical of southern latitudes and a decrease for those more common in northern latitudes is observed in all populations. These changes could be due to climatic factors that are correlated with latitude, making the chromosomal composition of this species more “southern.”

CLINES OF CHROMOSOMAL ARRANGEMENTS OF DROSOPHILA SUBOBSCURA IN SOUTH AMERICA EVOLVE CLOSER TO OLD WORLD PATTERNS

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Colonization of America by Drosophila subobscura: Heterotic effect of chromosomal arrangements revealed by the persistence of lethal genes

About 20 years ago Drosophila subobscura, a native Palearctic species, colonized both North and South America. In Palearctic populations lethal genes are not associated in general with particular chromosomal arrangements. In colonizing populations they are not randomly distributed and usually are associated to a different degree with chromosomal arrangements caused by the founder event. The persistence of two lethal genes in the colonizing populations, one completely associated with the O5 inversion and the other partially associated with the O3+4+7 arrangement, has been analyzed. In all populations studied (five North American and six South American) the observed frequency of the lethal gene completely associated with the O5 inversion is higher than expected, the difference being statistically significant in all South American and one North American populations. The observed frequency of the lethal gene partially associated with the O3+4+7 arrangement is also significantly higher than expected. Taking into account that the O5 inversion exhibits significant latitudinal clines both in North and South America, an overdominant model favoring the heterokaryotypes seems to be in operation. From this model, a polynomial expression has been developed that allows us to estimate the relative fitness and the coefficient of selection against all karyotypes not carrying the O5 inversion. The relative fitness of the O5 heterokaryotypes is higher in South American than in North American populations. Furthermore, the observed frequencies of the lethal genes studied are in general very close to those of the equilibrium. This case is an outstanding demonstration in nature of an heterotic effect of chromosomal segments associated with lethal genes on a large geographic scale.

INTERSPECIFIC LABORATORY COMPETITION OF THE RECENTLY SYMPATRIC SPECIES DROSOPHILA SUBOBSCURA AND DROSOPHILA PSEUDOOBSCURA

Abstract.—Drosophila subobscura and D. pseudoobscura are closely related species coexisting on the West Coast of North America, which was recently colonized by D. subobscura. In competition experiments with overlapping generations, D. subobscura is eliminated by D. pseudoobscura in a few generations at all four temperatures and two initial frequencies tested. Yet in one‐species cultures, D. subobscura thrives at all experimental conditions. Single‐generation competition experiments reveal lower survivorship and productivity of D. subobscura at all temperatures and frequencies. Productivity per female is dependent on the initial frequencies: greater for D. subobscura as its initial frequency becomes higher, but lower for D. pseudoobscura as its frequency becomes higher. Strains of D. subobscura from three disparate geographic origins yield similar results.

Interspecific Competition in the Laboratory between Drosophila subobscura and D. azteca

Abstract Drosophila subobscura and D. azteca are closely related species that have coexisted on the west coast of North America since that area was colonized by D. subobscura in the late 1970s. We have studied competition between the two species by the serial transfer technique at different initial proportions (20%, 50%, 80% and 100%) and at two densities (20 and 100 individuals). The cultures were maintained at 18 C. In the mixed cultures D. subobscura outcompeted D. azteca at both densities and all initial proportions. Survivorship was similar for both species, although the productivity of D. azteca was reduced, especially in the mixed cultures. The productivity of D. subobscura in the mixed cultures was a function only of the initial number of individuals of this species, and was completely unaffected by the number of D. azteca in the populations. Carrying capacity was attained by both species when the number of founder individuals was twenty; however, the number of descendants was much lower for D. azteca than for D. subobscura. In the pure cultures an important effect of season was detected in the replicates: the productivity of D. subobscura was much higher in spring than in autumn, while the reverse was observed in D. azteca. This effect was not detected in the mixed populations. Thus, lower carrying capacity, lower fecundity, longer mean eclosion rate, delayed oviposition or a combination of all of them could explain the low success of D. azteca in the mixed cultures.

Analysis of inbreeding in a colonizing population of Drosophila subobscura

An analysis of the effects of inbreeding on the genetic structure of a colonizing population of Drosophila subobscura has been carried out. Species of Drosophila, particularly D. subobscura, may have lethal alleles associated with chromosomal inversions and our aim was to assess the extent to which the genome is balanced in this way. The frequencies of chromosomal inversions were compared between a large population and a set of 72 lines that were maintained by brother-sister mating for 10 generations. Fishers matrix method was used to calculate the expected homozygosity in these inbred lines for 5 allozyme loci (Aph, Hk-1, Lap, Odh, and Pept-1) used as markers of large chromosomal segments. Furthermore, the expected rates of fixation corresponding to these allozyme loci were also calculated. The results show that the amount of homozygosis observed did not differ significantly from expectations (with the corresponding loss of lines as a consequence of the reduction in viability). However, two deviations from strict neutrality were observed: there was a heterozygote excess at the Lap locus, and the frequency of the O5 inversion (always associated with a lethal gene in colonizing populations) was higher than expected.