Can selection on a male mating character result in evolutionary change? A selection experiment on California wild radish, <i>Raphanus sativus</i>

Marshall, Diane L.; Evans, Ann S.

doi:10.3732/ajb.1500171

Cited by 14 publications

(16 citation statements)

References 169 publications

(241 reference statements)

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“…A recent selection study in wild radish for three generations on the capacity of pollen to sire seeds either at the top or basal position of fruits, where the latter is associated with faster growing pollen tubes, resulted in evolution of more competitive pollen in plants generated from the basal fruit position in two out of four replicates (Marshall and Evans 2016). A difference between their study and the present study is that we did not select directly on pollen traits, but rather created an environment-protandry-that favored high early fertilization and fast pollen tube growth rate.…”

Section: Discussionmentioning

confidence: 99%

Sexually antagonistic evolution caused by male-male competition in the pistil

2017

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Although sexual selection and sexual conflict are important evolutionary forces in animals, their significance in plants is uncertain. In hermaphroditic organisms, such as many plants, sexual conflict may occur both between mating partners (interlocus conflict) and between male and female sex roles within an individual (intralocus conflict). We performed experimental evolution, involving lines that were crossed with either one or two pollen donors (monogamous or polyandrous lines), in the hermaphroditic plant (Collinsia heterophylla) where early fertilizations are associated with female fitness costs (reduced seed set). Artificial polyandry for four generations resulted in enhanced pollen performance and increased female fitness costs compared to the monogamous and source (starting material) lines. Female fitness was also reduced in the monogamous line, indicating a possible trade-off between sex roles, resulting from early pollination. We performed a second experiment to investigate a potential harming effect of pollen performance on seed set. We found that high siring success of early arriving pollen competing with later-arriving pollen was associated with high female fitness costs, consistent with an interlocus sexual conflict. Our study provides evidence for the importance of sexual selection in shaping evolution of plant reproductive strategies, but also pinpoints the complexity of sexual conflict in hermaphroditic species.

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Section: Discussionmentioning

confidence: 99%

Sexually antagonistic evolution caused by male-male competition in the pistil

2017

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“…To the extent that pollen and sperm success reflects differences in their haploid genotypes, competition among these gametes/gametophytes is qualitatively distinct from selection among diploid males (Immler et al 2012). In plants, selection among haploid male gametophytes is thought to be pervasive (Skogsmyr and Lankinen 2002;Moore and Pannell 2011;Marshall and Evans 2016); in Arabidopsis, 60-70% of all genes are expressed during the haploid phase (Borg et al 2009), and pollen-expressed genes exhibit stronger signatures of purifying selection and positive selection (Arunkumar et al 2013;Gossmann et al 2014). For agricultural breeding, pollen has been exposed to a variety of selection pressures in vivo and in vitro, including temperature (Clarke et al 2004;Hedhly et al 2004), herbicides (Frascaroli and Songstad 2001), metals (Searcy and Mulcahy 1985), water stress (Ravikumar et al 2003), and pathogens (Ravikumar et al 2012), resulting in an increased frequency of beneficial genotypes among the diploid sporophytic offspring.…”

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confidence: 99%

Haploid Selection Favors Suppressed Recombination Between Sex Chromosomes Despite Causing Biased Sex Ratios

Scott

Otto

2017

Genetics

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To date, research on the evolution of sex chromosomes has focused on sexually antagonistic selection among diploids, which has been shown to be a potent driver of the strata and reduced recombination that characterize many sex chromosomes. However, significant selection can also occur on haploid genotypes during less conspicuous life cycle stages, , competition among sperm/pollen or meiotic drive during gamete/spore production. These haploid selective processes are typically sex-specific,, gametic/gametophytic competition typically occurs among sperm/pollen, and meiotic drive typically occurs during either spermatogenesis or oogenesis. We use models to investigate whether sex-specific selection on haploids could drive the evolution of recombination suppression on the sex chromosomes, as has been demonstrated for sex-specific selection among diploids. A potential complication is that zygotic sex-ratios become biased when haploid selected loci become linked to the sex-determining region because the zygotic sex ratio is determined by the relative number and fitness of X- Y-bearing sperm. Despite causing biased zygotic sex-ratios, we find that a period of sex-specific haploid selection generally favors recombination suppression on the sex chromosomes. Suppressed recombination is favored because it allows associations to build up between haploid-beneficial alleles and the sex that experiences haploid selection most often (, pollen beneficial alleles become strongly associated with the male determining region, Y or Z). Haploid selected loci can favor recombination suppression even in the absence of selective differences between male and female diploids. Overall, we expand our view of the sex-specific life cycle stages that can drive sex chromosome evolution to include gametic competition and meiotic drive. Based on our models, sex chromosomes should become enriched for genes that experience haploid selection, as is expected for genes that experience sexually antagonistic selection. Thus, we generate a number of predictions that can be evaluated in emerging sex chromosome systems.

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“…This context‐specific effect of pollen size on performance indicates that other factors, such as pollen–pistil interactions, pollen genotype × environment interactions, or other genetically based differences among pollen donors that influence pollen performance must also play a role in determining the outcome of these competitive interactions and in maintaining the high level of genetic variation in pollen grain size that made this elegant experiment possible in the first place. Marshall and Evans (2016 in this issue) also found a pollen size effect on pollen performance (see next section).…”

Section: What Specific Pollen Traits Affect Male Gametophyte Performamentioning

confidence: 72%

Pollen—Tiny and ephemeral but not forgotten: New ideas on their ecology and evolution

Williams

Mazer

2016

American J of Botany

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Ecologists and evolutionary biologists have been interested in the functional biology of pollen since the discovery in the 1800s that pollen grains encompass tiny plants (male gametophytes) that develop and produce sperm cells. After the discovery of double fertilization in flowering plants, botanists in the early 1900s were quick to explore the effects of temperature and maternal nutrients on pollen performance, while evolutionary biologists began studying the nature of haploid selection and pollen competition. A series of technical and theoretic developments have subsequently, but usually separately, expanded our knowledge of the nature of pollen performance and how it evolves. Today, there is a tremendous diversity of interests that touch on pollen performance, ranging from the ecological setting on the stigma, structural and physiological aspects of pollen germination and tube growth, the form of pollen competition and its role in sexual selection in plants, virus transmission, mating system evolution, and inbreeding depression. Given the explosion of technical knowledge of pollen cell biology, computer modeling, and new methods to deal with diversity in a phylogenetic context, we are now more than ever poised for a new era of research that includes complex functional traits that limit or enhance the evolution of these deceptively simple organisms.

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Can selection on a male mating character result in evolutionary change? A selection experiment on California wild radish, Raphanus sativus

Cited by 14 publications

References 169 publications

Sexually antagonistic evolution caused by male-male competition in the pistil

Sexually antagonistic evolution caused by male-male competition in the pistil

Haploid Selection Favors Suppressed Recombination Between Sex Chromosomes Despite Causing Biased Sex Ratios

Pollen—Tiny and ephemeral but not forgotten: New ideas on their ecology and evolution

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