The Effect of Temperature on Drosophila Hybrid Fitness

Abstract

Mechanisms of reproductive isolation inhibit gene flow between species and can be broadly sorted into two categories: prezygotic and postzygotic. While comparative studies suggest that prezygotic barriers tend to evolve first, postzygotic barriers are crucial for maintaining species boundaries and impeding gene flow that might otherwise cause incipient species to merge. Most, but not all, postzygotic barriers result from genetic incompatibilities between two or more loci from different species, and occur due to divergent evolution in allopatry. Hybrid defects result from improper allelic interactions between these loci. While some postzygotic barriers are environmentally-independent, the magnitude of others has been shown to vary in penetrance depending on environmental factors. We crossed Drosophila melanogaster mutants to two other species, D. simulans and D. santomea, and collected fitness data of the hybrids at two different temperatures. Our goal was to examine the effect of temperature on recessive incompatibility alleles in their genomes. We found that temperature has a stronger effect on the penetrance of recessive incompatibility alleles in the D. simulans genome than on those in the D. santomea genome. These results suggest that the penetrance of hybrid incompatibilities can be strongly affected by environmental context, and that the magnitude of such gene-by-environment interactions can be contingent on the genotype of the hybrid.

Keywords: Drosophila; hybrids; postzygotic isolation; temperature.

Figure 1

Deficiency mapping approach to detect alleles involved in hybrid inviability. A significant dearth of df/san individuals compared to their Bal/san sisters indicates that the deficiency uncovers a lethal or semilethal allele involved in hybrid inviability. D. melanogaster balancer chromosomes are shown as striped bars; deficiency chromosomes are shown as a line connecting two bars. D. santomea chromosomes are shown in light gray. Sex chromosomes are shown as shorter bars than autosomes, and Y is shown as shorter than the X. Bal, balancer chromosome; df, deficiencies; mel, D. melanogaster; san, D. santomea.

Figure 2

Deficiency mapping of hybrid incompatibilities in the D. santomea genome at two different temperatures. Light blue: hybrid inviability only at 18°. Green: hybrid inviability only at 24°. Dark blue: hybrid inviability at both temperatures. Deficiencies not causing hybrid inviability are not shown.

Figure 3

Relative fitness frequencies of the df-carrying hybrids in mel/san hybrids at two different temperatures. (A) mel/san 18°. (B) mel/san 24°. Black solid lines in each panel show the mean fitness of the df-carrying hybrids. Black dashed lines show the mean ± SD of the mean. The x-axis shows relative viability of deficiency-carrying progeny (observed df-carrying progeny/observed Bal-carrying progeny + observed df-carrying progeny) while the y-axis shows the number of stocks having a given level of viability of deficiency carrying offspring. Bal, balancer chromosome; df, deficiencies; mel, D. melanogaster; san, D. santomea.

Figure 4

Deficiency mapping of hybrid incompatibilities in the D. simulans genome at two different temperatures. Orange: hybrid inviability only at 18°. Pink: hybrid inviability only at 24°. Red: hybrid inviability at both temperatures. Deficiencies not causing hybrid inviability are not shown.

Figure 5

Fitness frequencies of the df-carrying hybrids in mel/sim hybrids at two different temperatures. (A) mel/sim 18°. (B) mel/sim 24°. Black solid lines in each panel show the mean fitness of the df-carrying hybrids. Black dashed lines show the average ± SD from the mean. The x-axis shows relative viability of deficiency-carrying progeny (observed df-carrying progeny/observed Bal-carrying progeny + observed df-carrying progeny) while the y-axis shows the number of stocks having a given level of viability of deficiency carrying offspring. Bal, balancer chromosome; df, deficiencies; mel, D. melanogaster; sim, D. simulans.