Selection on Plant Male Function Genes Identifies Candidates for Reproductive Isolation of Yellow Monkeyflowers

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.

Reproductive isolation and introgression between sympatricMimulusspecies

“…At least some of this distortion appears to be caused by loci that influence pollen performance (Aagaard et al . ), and M. guttatus alleles at such loci are expected to have a competitive advantage over inbred M. nasutus alleles (Brandvain & Haig ). Going forward, a key question is to what extent distortion against M. nasutus alleles in a heterospecific genetic background impedes introgression into M. guttatus at Catherine Creek.…”

Targeted capture in evolutionary and ecological genomics

“…Tests for selection based on protein divergence are appealing because they rely upon the well-established foundations of molecular evolution, are relatively robust to confounding demographic effects (Nielsen 2001), and enable functional inferences regarding the targets of selection. Targeted exome capture offers a highly cost-effective approach to extend these tests beyond classic model systems to a broader range of taxa (Burbano et al 2010; Aagard et al 2013; Vilstrup et al 2013; George et al 2011; Good et al 2013). For instance, George et al (2011) performed an exome capture of several Old and New World monkeys and revealed novel targets of positive selection on genes associated with keratinization or the conversion of epithelial cells to keratin.…”

“…For instance, George et al (2011) performed an exome capture of several Old and New World monkeys and revealed novel targets of positive selection on genes associated with keratinization or the conversion of epithelial cells to keratin. Moreover, comparative exome data can be used to move beyond the post hoc inferences provided by standard genome-wide scans for selection towards a priori hypothesis testing of specific genetic pathways or classes of genes (e.g., Smadja et al 2012; Nadeau et al 2012; Aagaard et al 2013; Good et al 2013). Thus, in addition to elucidating the frequency and mode of selection, comparative molecular evolutionary studies of targeted exome data can provide essential information on the ecological or life history drivers of molecular evolution.…”

“…While this level of population sampling is often not feasible with WGS or RNA-seq, exome capture provides a powerful platform to collect population-level genomic data. Targeted capture has frequently been used to estimate the efficacy of selection in populations (Hvilson et al 2012; Veeramah et al 2014; Bataillon et al 2015) and to infer local adaptation by identifying highly differentiated loci between populations (Yi et al 2010; Nadeau et al 2012; Smadja et al 2012; Hebert et al 2013; Müller et al 2014) or signatures of selective sweeps (Aagaard et al 2013; Linnen et al 2013; Tsangaras et al 2014). The potential power of capture-based population genomic studies is exemplified by Yi et al (2010) who used whole exome capture to investigate the genetic basis of high altitude adaptation in Tibetans.…”

Sexual selection in hermaphrodites, sperm and broadcast spawners, plants and fungi

“…Genes regulating elongation of pollen tube growth [104], and those that mask the effects of deleterious mutations (e.g. genes that are effectively diploid in the pollen tube such as flavonoids that speed up pollen tube growth [105]), are likely to play a major role in pollen endurance and viability, and ultimately in male-mating success [106]. In addition, changes to pollen coat, and to processes of communication between the pollen tube and style that can also affect reproductive compatibility between the sexes (e.g.…”