Genetic and Phenotypic Differentiation in Three Chromosomal Arrangements of Drosophila Subobscura.

Abstract

Background_x000D_ Global warming is affecting many wild species in different ways. One of the species demonstrating thermal adaptation on the population genetic level is Drosophila subobscura. Latitudinal clines in the frequency of many chromosomal inversions of this species were well documented in the original Palearctic populations, and the discovery of parallel clinal patterns a few years after the colonization of South and North Americas provided compelling evidence that the clines evolved by natural selection. However, the selective process maintaining inversions in populations is not yet clear. Traditionally three selective hypotheses have been advanced to explain the maintenance of the chromosomal polymorphism, according to the level of operation of natural selection: chromosome, coadapted genes (“supergenes”) and individual genes. _x000D_ Objectives_x000D_ To distinguish between different hypotheses the following aspects were studied in D. subobscura: _x000D_ 1. The distribution of chromosomal arrangements along the thermal gradient;_x000D_ 2. The nucleotide variation in six genes inside the three most frequent chromosomal inversions;_x000D_ 3. The genetic basis of thermal preference and heat shock tolerance in isochromosomal lines._x000D_ Results and conclusions_x000D_ The frequencies of the most abundant chromosomal arrangements in general correlated with temperature gradient, forming latitudinal clines. The arrangement OST positively correlated with latitude and its frequency increased from the south to the north. At the same time the frequency of O3+4+7 shows a negative correlation with latitude and reaches its maximum frequency in the south of Europe disappearing in the north. The O3+4 arrangement has a negative correlation with the latitude. Therefore, the arrangement OST is supposed to be cold-adapted while the other arrangements are considered to be warm-adapted._x000D_ The nucleotide variation of the most frequent chromosome arrangements was analyzed in two distant Spanish populations situated along a latitudinal gradient. No within-inversion genetic differences were detected among populations, which suggest that the gene content along the gradient is rather constant for the various chromosomal arrangements and genetic flow is high. Although gene flux between different inversions was detected, significant genetic differentiation among inversions for all genes was found. Genetic differentiation between arrangements was also detected by linkage disequilibrium analysis, showing significant associations between informative sites when comparing arrangement pairs, which could be explained by low recombination rate between inversions and probable epistasis between some genes. The footprints of selection nearly in all genes, either in coding or noncoding parts, were detected using several neutrality tests. The Local Adaptation hypothesis is the one that fits better to our data and would explain the maintenance of the coadapted gene complexes within inversions in D. subobscura. _x000D_ Our results corroborate that arrangements on chromosome O affect adult thermal preference in a laboratory temperature gradient, with cold-climate OST carriers displaying a lower thermal preference than their warm-climate O3+4 and O3+4+8 counterparts. However, these chromosome arrangements did not have any effect on adult heat tolerance and, hence, we putatively discard a genetic covariance between both traits arising from linkage disequilibrium between genes affecting thermal preference and genes of heat shock resistance. Therefore, thermal preference and heat tolerance in the isochromosomal lines of D. subobscura appear to be genetically independent, which might potentially prevent a coherent response of behavior and physiology (i.e., coadaptation) to thermal selection. If this pattern were general to all chromosomes, then any correlation between thermal preference and heat resistance across latitudinal gradients would likely reflect a pattern of correlated selection rather than genetic correlation.

Date of Award	16 Dec 2013
Original language	English
Supervisor	Mauro Santos Maroño (Director), Marta Pascual Berniola (Director) & Joan Balanya Maymó (Director)