We provide a partial test of the mitonuclear sex hypothesis with the first controlled study of how male frequencies and rates of outcrossing evolve in response to mitonuclear mismatch by allowing replicate lineages of C. elegans nematodes containing either mitochondrial or nuclear mutations of electron transport chain (ETC) genes to evolve under three sexual systems: facultatively outcrossing (wildtype), obligately selfing, and obligately outcrossing. Among facultatively outcrossing lines, we found evolution of increased male frequency in at least one replicate line of all four ETC mutant backgrounds tested—nuclear isp-1 , mitochondrial cox-1 and ctb-1 , and an isp-1 IV; ctb-1M mitonuclear double mutant—and confirmed for a single line set ( cox-1 ) that increased male frequency also resulted in successful outcrossing. We previously found the same result for lines evolved from another nuclear ETC mutant, gas-1 . For several lines in the current experiment, however, male frequency declined to wildtype levels (near 0%) in later generations. Male frequency did not change in lines evolved from a wildtype control strain. Additional phenotypic assays of lines evolved from the mitochondrial cox-1 mutant indicated that evolution of high male frequency was accompanied by evolution of increased male sperm size and mating success with tester females, but that it did not translate into increased mating success with coevolved hermaphrodites. Rather, hermaphrodites’ self-crossed reproductive fitness increased, consistent with sexually antagonistic coevolution. In accordance with evolutionary theory, males and sexual outcrossing may be most beneficial to populations evolving from a state of low ancestral fitness ( gas-1 , as previously reported) and less beneficial or deleterious to those evolving from a state of higher ancestral fitness ( cox-1 ). In support of this idea, the obligately outcrossing fog-2 V; cox-1 M lines exhibited no fitness evolution compared to their ancestor, while facultatively outcrossing lines showed slight upward evolution of fitness, and all but one of the obligately selfing xol-1 X; cox-1 M lines evolved substantially increased fitness—even beyond wildtype levels. This work provides a foundation to directly test the effect of reproductive mode on the evolutionary dynamics of mitonuclear genomes, as well as whether compensatory mutations (nuclear or mitochondrial) can rescue populations from mitochondrial dysfunction.
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Evolution of sex ratio through gene loss
The maintenance of males at intermediate frequencies is an important evolutionary problem. Several species of Caenorhabditis nematodes have evolved a mating system in which selfing hermaphrodites and males coexist. While selfing produces XX hermaphrodites, cross-fertilization produces 50% XO male progeny. Thus, male mating success dictates the sex ratio. Here, we focus on the contribution of the male secreted short (mss) gene family to male mating success, sex ratio, and population growth. The mss family is essential for sperm competitiveness in gonochoristic species, but has been lost in parallel in androdioecious species. Using a transgene to restore mss function to the androdioecious Caenorhabditis briggsae, we examined how mating system and population subdivision influence the fitness of the mss+ genotype. Consistent with theoretical expectations, when mss+ and mss-null (i.e., wild type) genotypes compete, mss+ is positively selected in both mixed-mating and strictly outcrossing situations, though more strongly in the latter. Thus, while sexual mode alone affects the fitness of mss+, it is insufficient to explain its parallel loss. However, in genetically homogenous androdioecious populations, mss+ both increases male frequency and depresses population growth. We propose that the lack of inbreeding depression and the strong subdivision that characterize natural Caenorhabditis populations impose selection on sex ratio that makes loss of mss adaptive after self-fertility evolves.
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- Award ID(s):
- 1755379
- NSF-PAR ID:
- 10109702
- Date Published:
- Journal Name:
- Proceedings of the National Academy of Sciences of the United States of America
- Volume:
- 116
- Issue:
- 26
- ISSN:
- 1091-6490
- Page Range / eLocation ID:
- 12919–12924
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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Abstract Selection that acts in a sex-specific manner causes the evolution of sexual dimorphism. Sex-specific phenotypic selection has been demonstrated in many taxa and can be in the same direction in the two sexes (differing only in magnitude), limited to one sex, or in opposing directions (antagonistic). Attempts to detect the signal of sex-specific selection from genomic data have confronted numerous difficulties. These challenges highlight the utility of “direct approaches,” in which fitness is predicted from individual genotype within each sex. Here, we directly measured selection on Single Nucleotide Polymorphisms (SNPs) in a natural population of the sexually dimorphic, dioecious plant, Silene latifolia. We measured flowering phenotypes, estimated fitness over one reproductive season, as well as survival to the next year, and genotyped all adults and a subset of their offspring for SNPs across the genome. We found that while phenotypic selection was congruent (fitness covaried similarly with flowering traits in both sexes), SNPs showed clear evidence for sex-specific selection. SNP-level selection was particularly strong in males and may involve an important gametic component (e.g., pollen competition). While the most significant SNPs under selection in males differed from those under selection in females, paternity selection showed a highly polygenic tradeoff with female survival. Alleles that increased male mating success tended to reduce female survival, indicating sexual antagonism at the genomic level. Perhaps most importantly, this experiment demonstrates that selection within natural populations can be strong enough to measure sex-specific fitness effects of individual loci.
Males and females typically differ phenotypically, a phenomenon known as sexual dimorphism. These differences arise when selection on males differs from selection on females, either in magnitude or direction. Estimated relationships between traits and fitness indicate that sex-specific selection is widespread, occurring in both plants and animals, and explains why so many species exhibit sexual dimorphism. Finding the specific loci experiencing sex-specific selection is a challenging prospect but one worth undertaking given the extensive evolutionary consequences. Flowering plants with separate sexes are ideal organisms for such studies, given that the fitness of females can be estimated by counting the number of seeds they produce. Determination of fitness for males has been made easier as thousands of genetic markers can now be used to assign paternity to seeds. We undertook just such a study in S. latifolia, a short-lived, herbaceous plant. We identified loci under sex-specific selection in this species and found more loci affecting fitness in males than females. Importantly, loci with major effects on male fitness were distinct from the loci with major effects on females. We detected sexual antagonism only when considering the aggregate effect of many loci. Hence, even though males and females share the same genome, this does not necessarily impose a constraint on their independent evolution.
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Sula granti ; a seabird) practise serial monogamy and biparental care. A male‐biased population sex ratio results in earlier and more frequent breeding by females. Based on sex‐specific reproductive schedules, females were expected to show faster age‐related decline for survival and reproduction. Within each sex, high reproductive effort in early life was expected to reduce late‐life performance and accelerate senescence.Longitudinal data were used to (a) evaluate the sex specificity of reproductive and actuarial senescence and then (b) test for early‐/late‐life fitness trade‐offs within each sex. Within‐sex analyses inform an interpretation of sex differences in senescence based on costs of reproduction. Analyses incorporated individual heterogeneity in breeding performance and cohort‐level differences in early‐adult environments.
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- Free Publicly Accessible Full Text
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Accepted Manuscript1.0
- Journal Article:
- https://doi.org/www.pnas.org/cgi/doi/10.1073/pnas.1903925116
