Periodic Reporting for period 4 - ComplexSex (Sex-limited experimental evolution of natural and novel sex chromosomes: the role of sex in shaping complex traits)
Okres sprawozdawczy: 2020-11-01 do 2022-04-30
The origin and evolution of sexual reproduction and sex differences represents one of the major unsolved problems in evolutionary biology. The standard model for sex chromosome evolution assumes that sexually antagonistic loci (genes with opposite fitness effects in males and female) accumulate near a novel sex determining locus, leading to suppression of recombination and eventual degeneration of the non-recombining chromosome (e.g. Y or W). Although much progress had been made both via theory and empirical research, recent data suggest that sex chromosome evolution may be more complex than previously thought, and the direct evidence that sexual antagonism is the driving force behind recombination cessation is surprisingly slim. This project therefore aimed to fill in the gaps in our knowledge about how the interacting effects of sex-linked genetic variation and sex-specific selection shape the genetic architecture of complex traits. A better understanding in this area can help us explain how and why sex differences evolve, which is important for a wide range of questions, including sex-specific adaptation to e.g. climate change, sex differences in disease prevalence and severity, and population divergence and speciation.
Main objectives:
1. To recreate in the lab three key points in the evolution of sex chromosomes: establishment of a new sex chromosome (WP4), between-population divergence of sex chromosomes (WP2), and within-population adaptation in a sex chromosome (WP1).
2. To test the hypothesis that sexually antagonistic loci are a key component in the above stages in sex chromosome evolution.
3. To test theoretical predictions about the relationship between individual sexually antagonistic loci and trait-level evidence for sexual antagonism.
These objectives were addressed by five work packages: female-limited X-chromosome evolution in Drosophila melanogaster, X-Y coevolution in Drosophila melanogaster, quantitative genetics of fitness in the hermaphrodite flatworm Macrostomum lignano, experimental evolution of a novel sex chromosome in Macrostomum lignano, and modelling of sexual antagonism in hermaphrodites and of sex chromosome evolution in general.
Main objectives:
1. To recreate in the lab three key points in the evolution of sex chromosomes: establishment of a new sex chromosome (WP4), between-population divergence of sex chromosomes (WP2), and within-population adaptation in a sex chromosome (WP1).
2. To test the hypothesis that sexually antagonistic loci are a key component in the above stages in sex chromosome evolution.
3. To test theoretical predictions about the relationship between individual sexually antagonistic loci and trait-level evidence for sexual antagonism.
These objectives were addressed by five work packages: female-limited X-chromosome evolution in Drosophila melanogaster, X-Y coevolution in Drosophila melanogaster, quantitative genetics of fitness in the hermaphrodite flatworm Macrostomum lignano, experimental evolution of a novel sex chromosome in Macrostomum lignano, and modelling of sexual antagonism in hermaphrodites and of sex chromosome evolution in general.
In WP1, we used a balancer chromosome to enforce matrilineal inheritance of the X chromosome, which eliminates male-specific selection and should result in feminization. We found evidence of phenotypic feminization in several traits, and genomic data suggested that in particular genes related to metabolism changed in expression. These changes seemed to result in a change in the genetic architecture, specifically a breakdown of the intersexual genetic correlation for locomotory activity. When females carrying one or two copies of an evolved X were compared, several phenotypic traits showed evidence of non-additivity. However, as work within WP1 progressed, it became clear that there were confounding effects of the FM balancer that was used to enforce matrilineal inheritance of the X chromosome, specifically increased female control over mating rates. Although initially disappointing, this discovery turned out to be highly interesting, since it allowed us to investigate the interactive effects of sexual antagonism and sexual conflict. By comparing the pattern of differences between the selection regimes, we were able to determine whether traits are mainly subject to sexual antagonism, sexual conflict, or a combination of the two.
In WP2 we were able to show that, surprisingly, males with mis-matched sex chromosomes had higher fitness than males with coevolved sex chromosomes. To follow up on this finding, we developed a novel mathematical model of coevolutionary cycles between the X and Y. We were able to show that coevolutionary cycles involving the X and Y chromosomes are favoured compared to coevolution between the Y and the autosomes.
In WP3 we found that there was indeed evidence of genetic variance for fitness in this species, but contrary to my initial expectation, there was no evidence of a negative genetic correlation fitness. We also carried out a follow-up experiment which found that variance in male fitness was increased under food restriction, while variance in female fitness was increased under osmotic stress.
In WP4 we carried out sex-limited selection in a hermaphrodite and found evidence of sexual specialization in gene expression, genital morphology, and behaviour, and metabolic gene expression. In addition, we found evidence of changes in recombination rate consistent with sexual specialization, which was an unexpected but highly interesting finding.
In WP5, we developed models of sexual antagonism in hermaphrodites as well as models of the establishment of inversions on sex chromosomes, and were able to show that different types of selective advantage give rise to different distributions of inversion sizes, but that they are dependent on the physical location of the sex determining locus. These models can now be combined with genomic data to test hypotheses about the evolution of recombination cessation.
The project has resulted in the production of 4 PhD theses, 8 papers, 2 preprints, and 2 other submitted manuscripts to date. A number of additional manuscripts are in preparation. Information about the results from the project has also been disseminated via national and international conferences. Finally, information has been disseminated to the public via several popular science lectures.
In WP2 we were able to show that, surprisingly, males with mis-matched sex chromosomes had higher fitness than males with coevolved sex chromosomes. To follow up on this finding, we developed a novel mathematical model of coevolutionary cycles between the X and Y. We were able to show that coevolutionary cycles involving the X and Y chromosomes are favoured compared to coevolution between the Y and the autosomes.
In WP3 we found that there was indeed evidence of genetic variance for fitness in this species, but contrary to my initial expectation, there was no evidence of a negative genetic correlation fitness. We also carried out a follow-up experiment which found that variance in male fitness was increased under food restriction, while variance in female fitness was increased under osmotic stress.
In WP4 we carried out sex-limited selection in a hermaphrodite and found evidence of sexual specialization in gene expression, genital morphology, and behaviour, and metabolic gene expression. In addition, we found evidence of changes in recombination rate consistent with sexual specialization, which was an unexpected but highly interesting finding.
In WP5, we developed models of sexual antagonism in hermaphrodites as well as models of the establishment of inversions on sex chromosomes, and were able to show that different types of selective advantage give rise to different distributions of inversion sizes, but that they are dependent on the physical location of the sex determining locus. These models can now be combined with genomic data to test hypotheses about the evolution of recombination cessation.
The project has resulted in the production of 4 PhD theses, 8 papers, 2 preprints, and 2 other submitted manuscripts to date. A number of additional manuscripts are in preparation. Information about the results from the project has also been disseminated via national and international conferences. Finally, information has been disseminated to the public via several popular science lectures.
Overall I believe that main general insight gained from the project is that experimental evolution can be valuable in testing theories of sex chromosome evolution. The majority of work on sex chromosome evolution is currently comparative in nature, e.g. using genomics to compare species of different relatedness. This approach has been very successful in demonstrating how much more variation there is in sex chromosome evolution than was anticipated. However a weakness of this approach is that it is impossible to disentangle cause and effect from stochastic changes.
In many cases we obtained results that were in line with our a priori predictions. However there are four main breakthroughs where I believe we have made progress beyond the state of the art:
1. The ability to determine whether traits are mainly subject to sexual antagonism, sexual conflict, or a combination of the two, is an important advance from WP1.
2. The finding that sexually antagonistic selection on different parts of the genome seems to have resulted in a breakdown of the intersexual genetic correlation for locomotory activity is another important advance from WP1. Our results provide an alternative explanation for the breakdown of intersexual genetic correlations which might be more easy to achieve in natural populations.
3. WP2 led to the development of a novel theoretical treatment of antagonistic coevolution on the sex chromosomes which should be testable in other systems.
4. Most of the results from WP4 fell in line with our a priori predictions, but it is significant as a successful proof of concept that experimental evolution can be used to study the early stages of sex chromosome evolution.
In many cases we obtained results that were in line with our a priori predictions. However there are four main breakthroughs where I believe we have made progress beyond the state of the art:
1. The ability to determine whether traits are mainly subject to sexual antagonism, sexual conflict, or a combination of the two, is an important advance from WP1.
2. The finding that sexually antagonistic selection on different parts of the genome seems to have resulted in a breakdown of the intersexual genetic correlation for locomotory activity is another important advance from WP1. Our results provide an alternative explanation for the breakdown of intersexual genetic correlations which might be more easy to achieve in natural populations.
3. WP2 led to the development of a novel theoretical treatment of antagonistic coevolution on the sex chromosomes which should be testable in other systems.
4. Most of the results from WP4 fell in line with our a priori predictions, but it is significant as a successful proof of concept that experimental evolution can be used to study the early stages of sex chromosome evolution.