Multiple Genes Cause Postmating Prezygotic Reproductive Isolation in theDrosophila virilisGroup

Abstract

Understanding the genetic basis of speciation is a central problem in evolutionary biology. Studies of reproductive isolation have provided several insights into the genetic causes of speciation, especially in taxa that lend themselves to detailed genetic scrutiny. Reproductive barriers have usually been divided into those that occur before zygote formation (prezygotic) and after (postzygotic), with the latter receiving a great deal of attention over several decades. Reproductive barriers that occur after mating but before zygote formation [postmating prezygotic (PMPZ)] are especially understudied at the genetic level. Here, I present a phenotypic and genetic analysis of a PMPZ reproductive barrier between two species of the Drosophila virilis group: D. americana and D. virilis. This species pair shows strong PMPZ isolation, especially when D. americana males mate with D. virilis females: ∼99% of eggs laid after these heterospecific copulations are not fertilized. Previous work has shown that the paternal loci contributing to this incompatibility reside on two chromosomes, one of which (chromosome 5) likely carries multiple factors. The other (chromosome 2) is fixed for a paracentric inversion that encompasses nearly half the chromosome. Here, I present two results. First, I show that PMPZ in this species cross is largely due to defective sperm storage in heterospecific copulations. Second, using advanced intercross and backcross mapping approaches, I identify genomic regions that carry genes capable of rescuing heterospecific fertilization. I conclude that paternal incompatibility between D. americana males and D. virilis females is underlain by four or more genes on chromosomes 2 and 5.

Evolutionary dynamics of male reproductive genes in theDrosophila virilissubgroup

“…virilis females is somewhat complex: at least three regions on the centromeric half of chromosome 5 (Muller C) and a large inversion on chromosome 2 (Muller E) carry genes responsible for the paternal component of PMPZ [2,49].…”

“…A striking pattern of PMPZ in this group is the strong incompatiblity between D. americana males and females from the sister species. Quantitative trait loci (QTL) that contribute to this paternal incompatibility between D. americana and D. virilis females have been mapped in two studies [2,49], and include a large inversion on chromosome 2 and several adjacent QTL on the centromeric half of chromosome 5. We found that the four SFPs with the highest ω values reside within the chromosome 2 inversion (Figure 7).…”

“…A subset of virilis group species (the D. virilis subgroup: D. americana, D. novamexicana, D. lummei, and D. virilis) show strong gametic incompatibilities in nearly all heterospecific hybridizations ( Figure S1B). In particular, five of the six heterospecific cross combinations between these species produce <2% hatched eggs in at least one direction of the cross [2,3,44,49]. The only species cross in which both directions show appreciable hatch rates is the cross between D. lummei and D. virilis (∼40% fertilization success).…”

“…The only species cross in which both directions show appreciable hatch rates is the cross between D. lummei and D. virilis (∼40% fertilization success). The reason for this general reduction in hatch rate was studied in three of these crosses, and appears mostly due to defects in sperm storage [2,3,44], but other postcopulatory defects are likely. Genetic analyses also reveal that the genetic architecture of the incompatibility between D. americana males and D.…”

Persistent postmating, prezygotic reproductive isolation between populations

“…For internal fertilizers, an additional array of potential PMPZ reproductive barriers can act as a result of the complex series of events that take place within the female reproductive tract after mating (Bloch Qazi, Heifetz, & Wolfner, 2003;Orr & Brennan, 2015;Schnakenberg, Siegal, & Bloch Qazi, 2012). In single heterospecific matings, successful fertilization can be decreased or prevented by reduced sperm transfer by males, and/or reduced transport, storage, and viability of hetero-specific sperm in females (Ahmed-Braimah, 2016;Kelleher & Markow, 2007;Kohyama, Matsubayashi, & Katakura, 2016;Larson, Hume, Andrés, & Harrison, 2012;Manier et al, 2013;Reinhardt, 2006;Rose, Brand, & Wilkinson, 2014). PMPZ isolation has also been suggested to occur when hetero-specific matings result in reduced egg production compared to con-specific matings, even though fertilization is successful (e.g., Matute & Coyne, 2010;Turissini, McGirr, Patel, David, & Matute, 2018).…”