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

Abstract

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.

Colonization of America by Drosophila subobscura: Association between Odh gene haplotypes, lethal genes and chromosomal arrangements

“…Thus, we have a natural experiment with two replicates (North and South America), with a very similar initial genetic variability and almost equivalent pattern of climates. However, the evolutionary processes have not been identical in both colonized areas: the heterotic effect of the O 5 inversion is different in both hemispheres (Mestres et al 2001) and the frequency clines of some chromosomal arrangements with latitude have not undergone the same evolutionary trajectories in both hemispheres (Balanyà et al 2003). There are likely to be important differences in both hemispheres with regard to some environmental conditions (physical and biological), for instance, there are other species of the obscura group in North America, but not in South America.…”

“…Furthermore, as only one haplotype has been detected in all American O 5 chromosomal inversions (which is completely associated with a lethal gene), the hypothesis that only one O 5 inversion was included in the initial sample of colonizers is confirmed . Thus, due to the founder effect, all O 5 inversions found in America are copies of the original inversion, which probably increased in frequency by genetic drift and natural selection (Mestres et al 2001).…”

“…These associations were found in both North and South American populations suggesting that the colonizations were not independent (Mestres et al 1992). Furthermore, the lethal genes have persisted in time, revealing a possible heterotic effect of these inversions (Mestres et al 2001). As the O 5 inversion is not very common and has a rather erratic distribution in the Old World Krimbas, 1993;Mestres et al 1994;Zivanovic and Mestres 2000), it is likely that only one O 5 inversion (carrying the lethal gene) was included in the initial sample of colonizers .…”

“…As the O 5 inversion is not very common and has a rather erratic distribution in the Old World Krimbas, 1993;Mestres et al 1994;Zivanovic and Mestres 2000), it is likely that only one O 5 inversion (carrying the lethal gene) was included in the initial sample of colonizers . The significant latitudinal clines of the frequency of this inversion observed in colonizing populations (Prevosti et al 1985;1990) together with its complete association with a lethal gene (Mestres et al 1990;, Solé et al 2000 and its significant persistence in America (Mestres et al 2001), make it especially suitable to study not only the origin of the colonization, but also some of the evolutionary consequences of this event.…”

The chromosomal polymorphism of Drosophila subobscura: a microevolutionary weapon to monitor global change

“…In fact, none of the 18 gene arrangements on either continent showed a significant increase in slope. We speculate that the shallower slope may be due to the more limited number of inversions, coupled with a general pattern of weak heterosis (Mestres et al, 2001): all else being equal, more gene arrangements for a given chromosome allow more ways to be a heterozygote. Coupled with graded selection pressures along the cline plus some gene flow, the fewer inversions would mean more shallow slopes.…”