Incipient Speciation by Sexual Isolation in Drosophila melanogaster: Extensive Genetic Divergence Without Reinforcement

Abstract

The collection of Drosophila melanogaster from Zimbabwe and nearby regions (the Z-type) yield females who would not mate with the cosmopolitan D. melanogaster males (the M-type). To dissect the genetic basis of this sexual isolation, we constructed 16 whole-chromosome substitution lines between two standard Z- and M-lines. The results were as follows: (1) All substitution lines appear normal in viability and fertility in both sexes, indicating no strong postmating isolation. (2) The genes for the behaviors are mapped to all three major chromosomes with the same ranking and comparable magnitude of effects for both sexes: III > II ⪢ X ≥ 0 (III, II and X designate the effects of the three chromosomes). The results suggest less evolution on the X than on autosomes at loci of sexual behavior. (3) The genes for “Z-maleness” are many and somewhat redundant. Whole-chromosome effects for Z-maleness appear nearly additive and show little dominance. (4) In contrast, “Z-femaleness” has less redundancy as partial genotypes never exhibit full phenotypic effects. Epistatic interactions and incomplete dominance can sometimes be detected. (5) The extensive genetic divergence underlying sexual isolation has evolved in the absence of detectable reduction in hybrid fitnesses. Sexual selection has apparently been a driving force of multiple facets of speciation at the nascent stage without reinforcement.

A shift to shorter cuticular hydrocarbons accompanies sexual isolation amongDrosophila americanagroup populations

“…These findings fit within a body of studies that have identified either male or female choice of sensory signals as critical for sexual isolation among Drosophila species (patterns reviewed Yukilevich and Patterson 2019). In Drosophila melanogaster , many studies have found that male choice of specific female CHC compounds play a role in isolation between closely related heterospecifics (Coyne et al 1995, Billeter et al 2009) as well as between intraspecific populations (Wu et al 1995, Hollocher et al 1997, Yukilevich and True 2008). Such patterns of CHC-mediated male mate-discrimination have also been associated with allelic variation in CHC elongases.…”

Patterns of and processes shaping population structure and introgression among recently differentiated Drosophila melanogaster populations

“…We next tested if patterns of diversity, differentiation, and population structure correspond to Z and M mating types within D. melanogaster (as described in [30, 32]). While Z mating behavior seems largely restricted to Subtropical Africa, previous work has identified that female mate choice is likely variable in the ancestral range of D. melanogaster [34] —however, the frequency of Z behavior within the ancestral range, as well as it’s phylogenetic distribution among Subtropical African flies, is largely unknown.…”

“…We used the aforementioned estimates of F ST calculated in 1KB windows between all Central Africa (including all lines, regardless of phenotype) and each OOA geographic region (Asia, Europe, North Africa, North America, and Tazmania), as well as F ST between Central Africa and each within-Africa geo-genetic lineage (West, East, Ethiopia, South, and HD). This analysis enabled us to determine whether Central Africa broadly shows increased differentiation for regions associated with female choosiness, in line with a polygenic genetic basis of female mate preference [30, 31]. We then performed an ANOVA with Type III SS to assess whether F ST differed between locus type (genome-wide versus behavioral PBE outlier), between comparison (each geographic region), and their interaction using the car package in R [57].…”

“…Cosmopolitan (denoted ‘M’) flies are globally distributed, including within Subtropical Africa, while a second lineage is largely restricted to Zambia and Zimbabwe (denoted ‘Z’). While Z females show significant preference for Z males, M females show no preference, and males of both lineages court both types of females at similar rates [30,32,34]. Early attempts to map the genetic basis of female preference found the trait to be highly polygenic, involving loci on all major chromosome arms, and significant non-additive effects [30, 31].…”

“…While Z females show significant preference for Z males, M females show no preference, and males of both lineages court both types of females at similar rates [30,32,34]. Early attempts to map the genetic basis of female preference found the trait to be highly polygenic, involving loci on all major chromosome arms, and significant non-additive effects [30, 31]. Despite the contributions of D. melanogaster to the field of speciation [35, 36], it remains unknown whether the frequencies of these behavioral types covary with patterns of D. melanogaster population structure within Subtropical Africa.…”