Abstract
Understanding the genetic basis of reproductive isolation promises insight into speciation and the origins of biological diversity. While progress has been made in identifying genes underlying barriers to reproduction that function after fertilization (post-zygotic isolation), we know much less about earlier acting pre-zygotic barriers. Of particular interest are barriers involved in mating and fertilization that can evolve extremely rapidly under sexual selection, suggesting they may play a prominent role in the initial stages of reproductive isolation. A significant challenge to the field of speciation genetics is developing new approaches for identification of candidate genes underlying these barriers, particularly among non-traditional model systems. We employ powerful proteomic and genomic strategies to study the genetic basis of conspecific pollen precedence, an important component of pre-zygotic reproductive isolation among yellow monkeyflowers (Mimulus spp.) resulting from male pollen competition. We use isotopic labeling in combination with shotgun proteomics to identify more than 2,000 male function (pollen tube) proteins within maternal reproductive structures (styles) of M. guttatus flowers where pollen competition occurs. We then sequence array-captured pollen tube exomes from a large outcrossing population of M. guttatus, and identify those genes with evidence of selective sweeps or balancing selection consistent with their role in pollen competition. We also test for evidence of positive selection on these genes more broadly across yellow monkeyflowers, because a signal of adaptive divergence is a common feature of genes causing reproductive isolation. Together the molecular evolution studies identify 159 pollen tube proteins that are candidate genes for conspecific pollen precedence. Our work demonstrates how powerful proteomic and genomic tools can be readily adapted to non-traditional model systems, allowing for genome-wide screens towards the goal of identifying the molecular basis of genetically complex traits.
Highlights
By identifying the genes underlying barriers to reproduction, we gain broad insight into the processes driving speciation and the origins of organismal diversity
We focus on identifying proteins of the male gametophyte with evidence of positive selection and/or rapid adaptive divergence as providing an opportunity to link molecular screens and conspecific pollen precedence (CPP) via the expectation that pollen competition reflects one or more components of sexual selection — an expectation which predicts sweeps and/or balancing selection for outcrossing populations of Mimulus, but which may be reflected in a signal of adaptive divergence over longer time scales among taxa of yellow monkeyflowers
Because we are able to match mass spectra for peptides corresponding to many thousands of proteins from pollinated styles using a similar level of MS/MS detection effort, this is strong evidence supporting successful 15N labeling of maternal style tissues and allows us to confidently identify pollen tube proteins (PTPs) within the style
Summary
By identifying the genes underlying barriers to reproduction, we gain broad insight into the processes driving speciation and the origins of organismal diversity. Reproductive barriers have long been known to include multiple pre-zygotic mechanisms that function before fertilization, after which post-zygotic barriers including hybrid sterility and inviability mark an irreversible stage of reproductive isolation [1]. Significant progress has been made in understanding the mechanisms that underlie post-zygotic isolating barriers, and in several cases the causal genes have been identified [2,3,4]. This work has had tremendous impact on our understanding of the genetic basis and evolutionary forces underlying hybrid sterility and inviability, in particular highlighting the important role of genetic conflicts and epistatic genic incompatibilities known as Bateson-Dobzhansky-Muller (BDM) incompatibilities [2]. Significantly less is known regarding the genes underlying earlier acting pre-zygotic barriers. As with classical examples of sexually selected traits [5], sexual selection even at a molecular level can be a strong force leading to the rapid evolution of reproductive barriers [6]
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