Abstract
BackgroundThe genetic basis of postzygotic isolation is a central puzzle in evolutionary biology. Evolutionary forces causing hybrid sterility or inviability act on the responsible genes while they still are polymorphic, thus we have to study these traits as they arise, before isolation is complete.Methodology/Principal FindingsIsofemale strains of D. mojavensis vary significantly in their production of sterile F1 sons when females are crossed to D. arizonae males. We took advantage of the intraspecific polymorphism, in a novel design, to perform quantitative trait locus (QTL) mapping analyses directly on F1 hybrid male sterility itself. We found that the genetic architecture of the polymorphism for hybrid male sterility (HMS) in the F1 is complex, involving multiple QTL, epistasis, and cytoplasmic effects.Conclusions/SignificanceThe role of extensive intraspecific polymorphism, multiple QTL, and epistatic interactions in HMS in this young species pair shows that HMS is arising as a complex trait in this system. Directional selection alone would be unlikely to maintain polymorphism at multiple loci, thus we hypothesize that directional selection is unlikely to be the only evolutionary force influencing postzygotic isolation.
Highlights
During the modern synthesis, Dobzhansky and Mayr proposed the Biological Species Concept that defines species by their ability to exchange genetic material within their group while being prevented from exchanging genetic material between groups [1,2]
Inbred D. mojavensis lines showing High and Low phenotypic levels of hybrid male sterility (HMS) when crossed to D. arizonae were used in a standard F2 intercross quantitative trait locus (QTL) mapping design (Figure 1)
A more complex basis, involving multiple loci and epistatic interactions? An earlier study [33] showed evidence of multiple polymorphic factors for HMS within D. mojavensis and additional data show genetic polymorphisms for HMS segregating in the sister species D. arizonae (Reed, unpublished)
Summary
Dobzhansky and Mayr proposed the Biological Species Concept that defines species by their ability to exchange genetic material within their group while being prevented from exchanging genetic material between groups [1,2]. Capturing the process of speciation early enough to determine the initial genetic causes of reproductive isolation, is challenging. A gap still remains in our understanding of the mechanisms underlying the very first stages of postzygotic isolation. Whether the genetic variation needed for postzygotic isolation is segregating within species in the form of epistatic variation [3,4] or instead arises as de novo mutations in allopatric populations [5] remains controversial. There is need for further empirical study to determine the roles of segregating and de novo polymorphism in speciation, and the underlying architecture of such variation [3]. Evolutionary forces causing hybrid sterility or inviability act on the responsible genes while they still are polymorphic, we have to study these traits as they arise, before isolation is complete
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