The Genetic Content of Chromosomal Inversions across a Wide Latitudinal Gradient

Chromosomal inversions are present in a wide range of animals and plants, having an important role in adaptation and speciation. Although empirical evidence of their adaptive value is abundant, the role of different processes underlying evolution of chromosomal polymorphisms is not fully understood. History and selection are likely to shape inversion polymorphism variation to an extent yet largely unknown. Here, we perform a real-time evolution study addressing the role of historical constraints and selection in the evolution of these polymorphisms. We founded laboratory populations of Drosophila subobscura derived from three locations along the European cline and followed the evolutionary dynamics of inversion polymorphisms throughout the first 40 generations. At the beginning, populations were highly differentiated and remained so throughout generations. We report evidence of positive selection for some inversions, variable between foundations. Signs of negative selection were more frequent, in particular for most cold-climate standard inversions across the three foundations. We found that previously observed convergence at the phenotypic level in these populations was not associated with convergence in inversion frequencies. In conclusion, our study shows that selection has shaped the evolutionary dynamics of inversion frequencies, but doing so within the constraints imposed by previous history. Both history and selection are therefore fundamental to predict the evolutionary potential of different populations to respond to global environmental changes.

Section: Discussionmentioning

confidence: 97%

How much can history constrain adaptive evolution? A real‐time evolutionary approach of inversion polymorphisms in Drosophila subobscura

Fragata

Lopes‐Cunha

Bárbaro

et al. 2014

“…The situation in D. subobscura is more complicated given the presence of extensive variation in chromosomal inversion polymorphisms that prevent recombination in inversion heterozygotes. Although there is gene flow within the same inversion arrangement (Simões et al ., ; Pegueroles et al ., ; Pratdesaba et al ., ), there is substantial evidence that inversion polymorphisms themselves are under selection (Balanyá et al ., ; Santos et al ., ).…”

Section: Discussionmentioning

confidence: 99%

Local adaptation of reproductive performance during thermal stress

Porcelli

Gaston

Butlin

et al. 2016

105

Considerable evidence exists for local adaptation of critical thermal limits in ectotherms following adult temperature stress, but fewer studies have tested for local adaptation of sublethal heat stress effects across life-history stages. In organisms with complex life cycles, such as holometabolous insects, heat stress during juvenile stages may severely impact gametogenesis, having downstream consequences on reproductive performance that may be mediated by local adaptation, although this is rarely studied. Here, we tested how exposure to either benign or heat stress temperature during juvenile and adult stages, either independently or combined, influences egg-to-adult viability, adult sperm motility and fertility in high-and low-latitude populations of Drosophila subobscura. We found both population-and temperaturespecific effects on survival and sperm motility; juvenile heat stress decreased survival and subsequent sperm motility and each trait was lower in the northern population. We found an interaction between population and temperature on fertility following application of juvenile heat stress; although fertility was negatively impacted in both populations, the southern population was less affected. When the adult stage was also subject to heat stress, the southern population exhibited positive carry-over effects whereas the northern population's fertility remained low. Thus, the northern population is more susceptible to sublethal reproductive consequences following exposure to juvenile heat stress. This may be common in other organisms with complex life cycles and current models predicting population responses to climate change, which do not take into account the impact of juvenile heat stress on reproductive performance, may be too conservative.

“…Similarly, regions of high linkage among loci within inversions interspersed with regions of low linkage (Kennington et al ., ) and linkage levels between loci not decreasing away from breakpoints (Munté et al ., ) have been interpreted as indicating selection acting against recombinants to maintain sets of co‐adapted genes. Nevertheless, several studies analysing the genetic differentiation of the same chromosomal arrangement between populations reported very low differentiation values, not expected under the co‐adaptation hypothesis (Rozas et al ., ; Schaeffer et al ., ; Simões et al ., ; Pegueroles et al ., ; but see Kennington & Hoffmann, ).…”

Section: Discussionmentioning

confidence: 99%

“…In Drosophila , high linkage disequilibrium patterns have been detected among genes within inversions, particularly near their breakpoints (Laayouni et al ., ; Schaeffer et al ., ; Nóbrega et al ., ; but see Munté et al ., ). This result is in agreement with the expectation that inverted segments reduce recombination, particularly near breakpoints in heterokaryotypes (Navarro et al ., ; Simões et al ., ). However, as both hypotheses lead to the expectation that selection favours certain combinations of genes within inverted regions, such finding does not allow discrimination between the two models.…”

Section: Introductionmentioning

confidence: 99%

“…() found a strong linkage between genes within chromosomal arrangements, away from breakpoints, interspersed with genes with low association, indicative of epistatic selection, as expected with Dobzhansky's model. Another expectation of the co‐adaptation hypothesis is that the same inversion will show genetic differentiation across populations, which does not seem to be the case according to most of the studies (Rozas et al ., ; Schaeffer et al ., ; Simões et al ., ; Pegueroles et al ., ; but see Kennington & Hoffmann, ).…”

Section: Introductionmentioning

confidence: 99%

See 1 more Smart Citation

Tracking changes in chromosomal arrangements and their genetic content during adaptation

Santos

Pascual

Fragata

et al. 2016

There is considerable evidence for an adaptive role of inversions, but how their genetic content evolves and affects the subsequent evolution of chromosomal polymorphism remains controversial. Here, we track how life-history traits, chromosomal arrangements and 22 microsatellites, within and outside inversions, change in three replicated populations of Drosophila subobscura for 30 generations of laboratory evolution since founding from the wild. The dynamics of fitness-related traits indicated adaptation to the new environment concomitant with directional evolution of chromosomal polymorphism. Evidence of selective changes in frequency of inversions was obtained for seven of 23 chromosomal arrangements, corroborating a role for inversions in adaptation. The evolution of linkage disequilibrium between some microsatellites and chromosomes suggested that adaptive changes in arrangements involved changes in their genetic content. Several microsatellite alleles increased in frequency more than expected by drift in targeted inversions in all replicate populations. In particular, there were signs of selection in the O3+4 arrangement favouring a combination of alleles in two loci linked to the inversion and changing along with it, although the lack of linkage disequilibrium between these loci precludes epistatic selection. Seven other alleles increased in frequency within inversions more than expected by drift, but were not in linkage disequilibrium with them. Possibly these alleles were hitchhiking along with alleles under selection that were not specific to those inversions. Overall, the selection detected on the genetic content of inversions, despite limited coverage of the genome, suggests that genetic changes within inversions play an important role in adaptation.