scholarly journals Genomic signatures of sexual selection on pollen-expressed genes in Arabis alpina

2021 ◽  
Author(s):  
Juanita Gutiérrez-Valencia ◽  
Marco Fracassetti ◽  
Robert Horvath ◽  
Benjamin Laenen ◽  
Aurélie Désamore ◽  
...  

Fertilization in angiosperms involves the germination of pollen on the stigma, followed by the extrusion of a pollen tube that elongates through the style and delivers two sperm cells to the embryo sac. Sexual selection could occur throughout this process when male gametophytes compete for fertilization. The strength of sexual selection during pollen competition should be affected by the number of genotypes deposited on the stigma. As increased self-fertilization reduces the number of mating partners, and the genetic diversity and heterozygosity of populations, it should thereby reduce the intensity of sexual selection during pollen competition. Despite the prevalence of mating system shifts, few studies have directly compared the molecular signatures of sexual selection during pollen competition in populations with different mating systems. Here we analyzed whole-genome sequences from natural populations of Arabis alpina, a species showing mating system variation across its distribution, to test whether shifts from cross- to self-fertilization result in molecular signatures consistent with sexual selection on genes involved in pollen competition. We found evidence for efficient purifying selection on genes expressed in vegetative pollen, and overall weaker selection on sperm-expressed genes. This pattern was robust when controlling for gene expression level and specificity. In agreement with the expectation that sexual selection intensifies under cross-fertilization, we found that the efficacy of purifying selection on male gametophyte-expressed genes was significantly stronger in genetically more diverse and outbred populations. Our results show that intra-sexual competition shapes the evolution of pollen-expressed genes, and that its strength fades with increasing self-fertilization rates.

Author(s):  
Juanita Gutiérrez-Valencia ◽  
Marco Fracassetti ◽  
Robert Horvath ◽  
Benjamin Laenen ◽  
Aurélie Désamore ◽  
...  

Abstract Fertilization in angiosperms involves the germination of pollen on the stigma, followed by the extrusion of a pollen tube that elongates through the style and delivers two sperm cells to the embryo sac. Sexual selection could occur throughout this process when male gametophytes compete for fertilization. The strength of sexual selection during pollen competition should be affected by the number of genotypes deposited on the stigma. As increased self-fertilization reduces the number of mating partners, and the genetic diversity and heterozygosity of populations, it should thereby reduce the intensity of sexual selection during pollen competition. Despite the prevalence of mating system shifts, few studies have directly compared the molecular signatures of sexual selection during pollen competition in populations with different mating systems. Here we analyzed whole-genome sequences from natural populations of Arabis alpina, a species showing mating system variation across its distribution, to test whether shifts from cross- to self-fertilization result in molecular signatures consistent with sexual selection on genes involved in pollen competition. We found evidence for efficient purifying selection on genes expressed in vegetative pollen, and overall weaker selection on sperm-expressed genes. This pattern was robust when controlling for gene expression level and specificity. In agreement with the expectation that sexual selection intensifies under cross-fertilization, we found that the efficacy of purifying selection on male gametophyte-expressed genes was significantly stronger in genetically more diverse and outbred populations. Our results show that intra-sexual competition shapes the evolution of pollen-expressed genes, and that its strength fades with increasing self-fertilization rates.


2017 ◽  
Author(s):  
Benjamin Laenen ◽  
Andrew Tedder ◽  
Michael D. Nowak ◽  
Per Toräng ◽  
Jörg Wunder ◽  
...  

Plant mating systems have profound effects on levels and structuring of genetic variation, and can affect the impact of natural selection. While theory predicts that intermediate outcrossing rates may allow plants to prevent accumulation of deleterious alleles, few studies have empirically tested this prediction using genomic data. Here, we study the effect of mating system on purifying selection by conducting population genomic analyses on whole-genome resequencing data from 38 European individuals of the arctic-alpine crucifer Arabis alpina. We find that outcrossing and mixed-mating populations maintain genetic diversity at similar levels, whereas highly self-fertilizing Scandinavian A. alpina show a strong reduction in genetic diversity, most likely as a result of a postglacial colonization bottleneck. We further find evidence for accumulation of genetic load in highly self-fertilizing populations, whereas the genome-wide impact of purifying selection does not differ greatly between mixed-mating and outcrossing populations. Our results demonstrate that intermediate levels of outcrossing may allow efficient selection against harmful alleles whereas demographic effects can be important for relaxed purifying selection in highly selfing populations. Thus, both mating system and demography shape the impact of purifying selection on genomic variation in A. alpina. These results are important for an improved understanding of the evolutionary consequences of mating system variation and the maintenance of mixed-mating strategies.SignificanceIntermediate outcrossing rates are theoretically predicted to maintain effective selection against harmful alleles, but few studies have empirically tested this prediction using genomic data. We used whole-genome resequencing data from alpine rock-cress to study how genetic variation and purifying selection vary with mating system. We find that populations with intermediate outcrossing rates have similar levels of genetic diversity as outcrossing populations, and that purifying selection against harmful alleles is efficient in mixed-mating populations. In contrast, self-fertilizing populations from Scandinavia have strongly reduced genetic diversity, and accumulate harmful mutations, likely as a result of demographic effects of postglacial colonization. Our results suggest that mixed-mating populations can avoid the negative evolutionary consequences of high self-fertilization rates.


2019 ◽  
Author(s):  
Åsa Lankinen ◽  
Maria Strandh

AbstractPremise of the ResearchThe wide diversity of floral traits seen among plants is shaped by neutral and selective evolutionary processes. In outcrossing species, sexual selection from competing pollen donors is expected to be important for shaping mating system-related traits but empirical evidence is scarce. In a previous evaluation of experimental evolution lines crossed with either one or two pollen donors (monogamous, M, or polyandrous, P, lines) at early floral stages in mixed-mating Collinsia heterophylla (Plantaginaceae), P showed enhanced pollen competitive ability and reduced maternal seed set compared to M, in accordance with sexually antagonistic evolution of pollen. Here, we asked whether the presence of sexual selection during pollen competition affect mating system-related floral traits in the same lines.MethodologyWe compared flowering start, timing of anther-stigma contact (as an indication of timing of self-pollination), timing of stigma receptivity and first seed set between M and P, and with a source line, S (starting material). The former three traits are later in outcrossers than in selfers of Collinsia. The latter trait was expected to be earlier in P than in M because of sexual selection for early seed siring of pollen.Pivotal ResultsArtificial polyandry for four generations resulted in later flowering start and later anther-stigma contact in P compared to M, and the latter trait was intermediate in S. Thus, P appeared more ‘outcrossing’ than M. Stigma receptivity did not differ between lines. First seed set was earlier in P than in M, as expected from sexual selection.ConclusionsOur results from C. heterophylla experimental evolution lines suggest that a component of sexual selection during outcross pollination could enhance the patterns of floral divergence commonly found between outcrossers and selfers.


2018 ◽  
Vol 115 (4) ◽  
pp. 816-821 ◽  
Author(s):  
Benjamin Laenen ◽  
Andrew Tedder ◽  
Michael D. Nowak ◽  
Per Toräng ◽  
Jörg Wunder ◽  
...  

Plant mating systems have profound effects on levels and structuring of genetic variation and can affect the impact of natural selection. Although theory predicts that intermediate outcrossing rates may allow plants to prevent accumulation of deleterious alleles, few studies have empirically tested this prediction using genomic data. Here, we study the effect of mating system on purifying selection by conducting population-genomic analyses on whole-genome resequencing data from 38 European individuals of the arctic-alpine crucifer Arabis alpina. We find that outcrossing and mixed-mating populations maintain genetic diversity at similar levels, whereas highly self-fertilizing Scandinavian A. alpina show a strong reduction in genetic diversity, most likely as a result of a postglacial colonization bottleneck. We further find evidence for accumulation of genetic load in highly self-fertilizing populations, whereas the genome-wide impact of purifying selection does not differ greatly between mixed-mating and outcrossing populations. Our results demonstrate that intermediate levels of outcrossing may allow efficient selection against harmful alleles, whereas demographic effects can be important for relaxed purifying selection in highly selfing populations. Thus, mating system and demography shape the impact of purifying selection on genomic variation in A. alpina. These results are important for an improved understanding of the evolutionary consequences of mating system variation and the maintenance of mixed-mating strategies.


2019 ◽  
Vol 20 (2) ◽  
pp. 420 ◽  
Author(s):  
Ren Zheng ◽  
Shun Su ◽  
Hui Xiao ◽  
Hui Tian

Pollen is the male gametophyte of higher plants. Its major function is to deliver sperm cells to the ovule to ensure successful fertilization. During this process, many interactions occur among pollen tubes and pistil cells and tissues, and calcium ion (Ca2+) dynamics mediate these interactions among cells to ensure that pollen reaches the embryo sac. Although the precise functions of Ca2+ dynamics in the cells are unknown, we can speculate about its roles on the basis of its spatial and temporal characteristics during these interactions. The results of many studies indicate that calcium is a critical element that is strongly related to pollen germination and pollen tube growth.


BMC Biology ◽  
2021 ◽  
Vol 19 (1) ◽  
Author(s):  
William Toubiana ◽  
David Armisén ◽  
Corentin Dechaud ◽  
Roberto Arbore ◽  
Abderrahman Khila

Abstract Background Exaggerated secondary sexual traits are widespread in nature and often evolve under strong directional sexual selection. Although heavily studied from both theoretical and empirical viewpoints, we have little understanding of how sexual selection influences sex-biased gene regulation during the development of exaggerated secondary sexual phenotypes, and how these changes are reflected in genomic architecture. This is primarily due to the limited availability of representative genomes and associated tissue and sex transcriptomes to study the development of these traits. Here we present the genome and developmental transcriptomes, focused on the legs, of the water strider Microvelia longipes, a species where males exhibit strikingly long third legs compared to females, which they use as weapons. Results We generated a high-quality genome assembly with 90% of the sequence captured in 13 scaffolds. The most exaggerated legs in males were particularly enriched in both sex-biased and leg-biased genes, indicating a specific signature of gene expression in association with trait exaggeration. We also found that male-biased genes showed patterns of fast evolution compared to non-biased and female-biased genes, indicative of directional or relaxed purifying selection. By contrast to male-biased genes, female-biased genes that are expressed in the third legs, but not the other legs, are over-represented in the X chromosome compared to the autosomes. An enrichment analysis for sex-biased genes along the chromosomes revealed also that they arrange in large genomic regions or in small clusters of two to four consecutive genes. The number and expression of these enriched regions were often associated with the exaggerated legs of males, suggesting a pattern of common regulation through genomic proximity in association with trait exaggeration. Conclusion Our findings indicate how directional sexual selection may drive sex-biased gene expression and genome architecture along the path to trait exaggeration and sexual dimorphism.


1977 ◽  
Vol 30 (4) ◽  
pp. 337 ◽  
Author(s):  
MA Phillips ◽  
AHD Brown

Allozyme polymorphisms at four loci expressed in seeds, and three other loci expressed in seedlings, were used to determine the outcrossing rate in three natural subalpine populations of snow gum (E. paucijlora). Based on the seed loci data, an estimated 37 % of seed was derived from self-fertilization and 63 % from random outcrossing. In the most elevated population the estimate after germination was similar. However, at lower elevations the frequency of effective self-fertilization estimated at the seedling stage was only 16 %. The less elevated populations also showed a greater average heterozygosity and a larger increase in heterozygosity in the adult over the progeny stages. Heterosis apparently operated differentially in these populations-it was more intense at the lower altitudes. Selection in favour of outcrossed individuals may be an important factor in checking the spread through the population of genes which promote self-fertilization, and which would otherwise enjoy an evolutionary advantage.


2021 ◽  
Vol 9 ◽  
Author(s):  
Theodora Fuss

The idea of “smart is sexy,” meaning superior cognition provides competitive benefits in mate choice and, therefore, evolutionary advantages in terms of reproductive fitness, is both exciting and captivating. Cognitively flexible individuals perceive and adapt more dynamically to (unpredictable) environmental changes. The sex roles that females and males adopt within their populations can vary greatly in response to the prevalent mating system. Based on how cognition determines these grossly divergent sex roles, different selection pressures could possibly shape the (progressive) evolution of cognitive abilities, suggesting the potential to induce sexual dimorphisms in superior cognitive abilities. Associations between an individual’s mating success, sexual traits and its cognitive abilities have been found consistently across vertebrate species and taxa, providing evidence that sexual selection may well shape the supporting cognitive prerequisites. Yet, while superior cognitive abilities provide benefits such as higher feeding success, improved antipredator behavior, or more favorable mate choice, they also claim costs such as higher energy levels and metabolic rates, which in turn may reduce fecundity, growth, or immune response. There is compelling evidence in a variety of vertebrate taxa that females appear to prefer skilled problem-solver males, i.e., they prefer those that appear to have better cognitive abilities. Consequently, cognition is also likely to have substantial effects on sexual selection processes. How the choosing sex assesses the cognitive abilities of potential mates has not been explored conclusively yet. Do cognitive skills guide an individual’s mate choice and does learning change an individual’s mate choice decisions? How and to which extent do individuals use their own cognitive skills to assess those of their conspecifics when choosing a mate? How does an individual’s role within a mating system influence the choice of the choosing sex in this context? Drawing on several examples from the vertebrate world, this review aims to elucidate various aspects associated with cognitive sex differences, the different roles of males and females in social and sexual interactions, and the potential influence of cognition on mate choice decisions. Finally, future perspectives aim to identify ways to answer the central question of how the triad of sex, cognition, and mate choice interacts.


2006 ◽  
Vol 274 (1609) ◽  
pp. 521-525 ◽  
Author(s):  
Charlotta Kvarnemo ◽  
Glenn I Moore ◽  
Adam G Jones

Studies of sexual selection in monogamous species have hitherto focused on sexual selection among males. Here, we provide empirical documentation that sexual selection can also act strongly on females in a natural population with a monogamous mating system. In our field-based genetic study of the monogamous Western Australian seahorse, Hippocampus subelongatus , sexual selection differentials and gradients show that females are under stronger sexual selection than males: mated females are larger than unmated ones, whereas mated and unmated males do not differ in size. In addition, the opportunity for sexual selection (variance in mating success divided by its mean squared) for females is almost three times that for males. These results, which seem to be generated by a combination of a male preference for larger females and a female-biased adult sex ratio, indicate that substantial sexual selection on females is a potentially important but under-appreciated evolutionary phenomenon in monogamous species.


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