Francesc Mestres

Introduction history of Drosophila subobscura in the New World: a microsatellite-based survey using ABC methods.

Drosophila subobscura is a Palearctic species that was first observed in South and North America in the early 1980s, and that rapidly invaded broad latitudinal ranges on both continents. To trace the source and history of this invasion, we obtained genotypic data on nine microsatellite loci from two South American, two North American and five European populations of D. subobscura. We analysed these data with traditional statistics as well as with an approximate Bayesian computation (ABC) framework. ABC methods yielded the strongest support for the scenario involving a serial introduction with founder events from Europe into South America, and then from South America into North America. Stable effective population size of the source population was very large (around one million individuals), and the propagule size was notably smaller for the introduction into South America (i.e. high bottleneck severity index with only a few effective founders) but considerably larger for the subsequent introduction into North America (i.e. low bottleneck severity index with around 100–150 effective founders). Finally, the Mediterranean region of Europe (and most likely Barcelona from the localities so far analysed) is proposed as the source of the New World flies, based on mean individual assignment statistics.

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.

COLONIZATION OF AMERICA BY DROSOPHILA SUBOBSCURA: LETHAL GENES AND THE PROBLEM OF THE O5 INVERSION

In this work, the process of colonization of North and South America by the species Drosophila subobscura has been studied by analyzing the variability of lethal genes. The genetic structures of a Palearctic natural central population (Bordils, Spain) and a colonizer population from America (Gilroy, California) have been compared. The frequencies of lethal chromosomes and their allelism are 29.007% and 0.0069 in the first population and 14.414% and 0.0526 in the American population. A founder effect is detected after the computation of some population parameters (Ne, h, he and the lethal load). Furthermore, the allelism of lethal chromosomes has revealed a strong association between a lethal gene and the O5 inversion both in Gilroy and in the population of Puerto Montt (Chile). The interpopulation allelism shows that the O5 arrangement from the USA and Chile is the same, confirming that the colonizing processes of North and South America are correlated. The O5 arrangement can also be useful as a genetic marker to trace the origin of the colonization. The frequency of the O5 arrangement in the original population of the colonization could be used to estimate the number of colonizers. This population is still unknown, but taking the extreme values of the frequency of the O5 inversion in natural Palearctic populations (1–15%), the number of colonizers could vary between 9 and 149 individuals.

Colonization of America by Drosophila subobscura : analysis of the O5 inversions from Europe and America and their implications for the colonizing process

The American colonization by the Palearctic species D. subobscura has been studied at the biogeographical, ecological and genetic levels (Bmcic et al., 1981; Prevosti et al., 1983, 1985, 1988, 1990; Beckenbach and Prevosti, 1986; Latorre et al., 1986; Ayala et al., 1989; Rozas and Aguade, 1991). In the present study we will focus on the variability of lethal genes and their allelism. The first studies at this level carried out in American populations of D. subobscura (Gilroy, California and Puerto Montt, Chile) have shown a strong association between a lethal gene and the 05 chromosomal inversion (Prevosti et al., 1989; Mestres et al., 1990). All 05 inversions so far analyzed in America are associated with the same lethal gene. Therefore, this lethal gene probably arose in the original Palearctic population and only one 05 inversion carrying this lethal gene reached America. Thus, the populations from North and South America would derive from the same original colonizing sample. Assuming that not all the European 05 inversions are associated with this lethal gene, the finding of this association in one European population would suggest that it was the population from which the colonization probably started. If the population of origin were detected, it would be possible to estimate the number of colonizers. We have analyzed samples of D. subobscura along a latitudinal cline in Europe to find 05 inversions and study their viabilities. Those that proved to be lethal were used to analyze the lethal allelism with the 05 inversions from America (both, from Gilroy and from Puerto Montt). Furthermore, an additional Chilean population (Santiago de Chile, located 900 km north of Puerto Montt) was analyzed to establish whether there was interpopulational allelism for other lethal genes in addition to that associated with the 05 inversion both in North and South America. Finally, the cytological pairing between the 05 inversions from Europe and from America was analyzed to determine their similarity at this level of observation.

Recombination and selection in the maintenance of the adaptive value of inversions

A huge amount of data seem to confirm the adaptive value of inversions in Drosophila. The inhibition of recombination in heterokaryotypes mediated by inversions seems fundamental in maintaining their adaptive role. This study shows that recombination is highly suppressed in Drosophila subobscura because of chromosomal inversions, not only inside the inversions but also outside them. It seems that the region outside the inversion where recombination is inhibited is asymmetrical and independent of the inversion length. Despite the difficulty of crossovers taking place near inversion breakpoints, the only two recombination events detected inside inversions were located close to the breakpoint. Thus, selection could be largely responsible for the recombination reduction maintaining sets of adaptive alleles inside the inverted region. Heterokaryotype descendants were always in higher frequency than inbred or outbred homokaryotypes, regardless of the geographical origin of the chromosome, suggesting that chromosomes carrying the same arrangement, although with a different set of alleles for neutral markers, could be submitted to the same selection processes.

Colonization and Establishment of the Paleartic Species Drosophila Subobscura in North and South America

Until 1978 Drosophila subobscura was a Palearctic species distributed all over Europe (except in Central and Northern Scandinavia), the Macaronesian Islands, North Africa and some parts of Western Asia. In most of this area it is a common species with rather dense populations. This species was detected for the first time in Chile in February 1978, in Puerto Montt in the South of the country (Brncic et al. 1981). Subsequently it has spread very quickly in Chile and in 1981 was present from La Serena (29°55′ LS) to Punta Arenas (53°10′ LS) (Budnik and Brncic 1982). In November 1981 we did find the species in large numbers in San Carlos de Bariloche (Argentina), east of the Andes (Prevosti et al. 1983). Later on, in November 1986, it was collected east of the Andes in Argentina from San Juan (31°33′ LS) to Esquel (42°55′ LS) (Table 1). A small and isolated collection by Lopez (1985) in Mar del Plata on the Atlantic Coast, about 400 km south of Buenos Aires, is the only finding of the species in other parts of Argentina. The same author (personal communication) did not find the species in other parts of the Buenos Aires province.

Gene flow and gene flux shape evolutionary patterns of variation in Drosophila subobscura

Gene flow (defined as allele exchange between populations) and gene flux (defined as allele exchange during meiosis in heterokaryotypic females) are important factors decreasing genetic differentiation between populations and inversions. Many chromosomal inversions are under strong selection and their role in recombination reduction enhances the maintenance of their genetic distinctness. Here we analyze levels and patterns of nucleotide diversity, selection and demographic history, using 37 individuals of Drosophila subobscura from Mount Parnes (Greece) and Barcelona (Spain). Our sampling focused on two frequent O-chromosome arrangements that differ by two overlapping inversions (OST and O3+4), which are differentially adapted to the environment as observed by their opposing latitudinal clines in inversion frequencies. The six analyzed genes (Pif1A, Abi, Sqd, Yrt, Atpα and Fmr1) were selected for their location across the O-chromosome and their implication in thermal adaptation. Despite the extensive gene flux detected outside the inverted region, significant genetic differentiation between both arrangements was found inside it. However, high levels of gene flow were detected for all six genes when comparing the same arrangement among populations. These results suggest that the adaptive value of inversions is maintained, regardless of the lack of genetic differentiation within arrangements from different populations, and thus favors the Local Adaptation hypothesis over the Coadapted Genome hypothesis as the basis of the selection acting on inversions in these populations.

Capacity of dispersal of a colonizing species: Drosophila subobscura

The European species Drosophila subobscura has colonized, in a very short time, large areas in South America (Chile and Argentina) and North America (The Pacific Coast, from Vancouver to Southern California), where it has been established as a very common species. Its capacity of dispersal was analyzed and results compared with the few data available from other authors. The estimates of the mean distance travelled during one activity period (159.20 meters) are considerably higher than those obtained by other authors. The Brownian motion model seems most probable because the values of σDF and σBM are very much alike. The effects on the estimates of some environmental factors, such as wind, are also discussed.

Changes in chromosomal polymorphism and global warming: the case of Drosophila subobscura from Apatin (Serbia)

In this study, chromosomal inversion polymorphism data for a natural population of Drosophila subobscura from a swampy region near the town of Apatin (Serbia) were compared with data for the same population collected approximately 15 years earlier. The pattern of chromosomal inversion polymorphism changed over time. There were significant increases in the frequency of characteristic southern latitude (“warm” adapted) chromosomal arrangements and significant decreases in the frequency of characteristic northern latitude (“cold” adapted) chromosomal arrangements in the O and U chromosomes. The chromosomal arrangements O3+4 and O3+4+22 (derived from the O3+4 arrangement) showed significant increases in 2008 and 2009 with regard to the 1994 sample. There was also a significant increase (∼50%) in the U1+2 arrangement, while U1+8+2 (a typical southern arrangement) was detected for the first time. Since the Apatin swampy population of D. subobscura has existed for a long time in a stable habitat with high humidity that has not been changed by man our results indicate that natural selection has produced chromosomal changes in response to the increase in temperature that has occurred in the Balkan Peninsula of central southeastern European.

Temporal and spatial genetic differentiation in the crab Liocarcinus depurator across the Atlantic-Mediterranean transition

Spatial genetic studies often require sampling broadly separated areas, difficult to access simultaneously. Although comparing localities surveyed at different time periods might result in spurious genetic differentiation, there is a general believe on the stability of genetic structure through time, particularly if sampled localities are isolated or very distant. By analysing spatial and temporal genetic differentiation of the portunid crab Liocarcinus depurator we assessed the contribution of historical and contemporary processes on population connectivity patterns across three main oceanographic discontinuities along the Atlantic-Mediterranean transition: Gibraltar Strait, Almeria-Oran Front and Ibiza Channel. A partial fragment of the cytochrome oxidase I gene was sequenced in 366 individuals collected from localities at both sides of each discontinuity during three time periods. Although localities showed genetic fluctuations through time, a significant gradient was detected along the coast for all sampling periods. Significant inter-annual differences identified within the Alicante area, north of the Almeria-Oran Front, were associated with shifts in the relative contribution of Atlantic and Mediterranean water masses. The persistence of a clinal pattern in the Atlantic-Mediterranean transition area together with local fluctuations suggests a complex balance of dispersal and selection.