The potential of inversions to accumulate balanced sexual antagonism is supported by simulations and Drosophila experiments

  1. Christopher S McAllester  Is a corresponding author
  2. John E Pool  Is a corresponding author
  1. Laboratory of Genetics, University of Wisconsin, United States
9 figures and 2 additional files

Figures

Conceptual representations of the proposed model of inversion-associated balanced sexual antagonism.

(A) Hypothetical skewed distribution of male mating success, yielding a greater variance in reproductive success for males than for females, such as expected under a ‘best of n’ mate choice model. (B

The layout of a single simulated generation.

Simulated individuals each reach the reproductive stage with probability in proportion to the product of the survival effects of their alleles. To generate each offspring in the next generation, a …

Figure 3 with 1 supplement
Simulations show that a balanced equilibrium frequency exists for certain sexually antagonistic variants.

The proportion of simulations retaining polymorphism (top) and the average final frequency (bottom) are plotted for a single locus at which there is one antagonistic allele with the indicated …

Figure 3—figure supplement 1
Single locus simulations under differing models exhibit shifts in the parameter combinations that produce balancing selection.

Each pixel in the heat-map plots represents 100 simulations of a population with a single polymorphic mutation of a given survival probability and display value that began at 0.5 frequency. Plots …

Figure 4 with 1 supplement
Simulated inversions may persist as polymorphisms when linked to sexually antagonistic, pleiotropic variants.

In turn, the presence of inversions facilitates the accumulation of antagonistic variation, demonstrating synergistic epistasis. Rates of long-term persistence are shown for simulations with two …

Figure 4—figure supplement 1
After 20 N generations of simulation, populations approach an equilibrium in which the haplotypes with both display-favoring or both survival-favoring variants are most fit, and selection removes recombinant haplotypes, maintaining high linkage.

(A) The number of descendant haplotypes per haplotype for each haplotype class averaged across all 1000 simulations, plotted for both sexes and within females and males separately. From the …

Simulated populations with stochastic mutation of new inversions and sexually antagonistic variants generate persistent inversion polymorphisms and accumulate linked sexually antagonistic variants.

(A) In simulated populations with stochastic mutation of new variants having pleiotropic effects on survival and male display, levels of antagonism increased with time before stabilizing at an …

Figure 6 with 1 supplement
Antagonism-associated karyotypes reach predictable equilibrium frequencies in simulations with antagonistic and inversion mutations, when survival costs are shared between sexes.

(A) Histograms of the number of karyotypic arrangements at a specified frequency across all simulation replicates in females (left) and males (right), colored by how the average survival effect of …

Figure 6—figure supplement 1
A histogram of the observed inversion frequencies in simulations with mutational generation of inversions with random position and length.

In these simulations, only one inversion was allowed per haplotype, to enable easier accounting of the average effects of variants associated with an arrangement. Without antagonistic mutations, or …

In simulations with female-limited survival costs, three distinct outcomes are observed involving either two or three balanced haplotypes.

From simulations with randomly occurring antagonistic and inversion mutations, histograms of inversion frequencies across simulations for surviving females (left) and males (right) are partitioned …

The layout and potential expectations of the laboratory evolution experiment.

We cross outbred males from a high-inversion population to inbred, non-inverted females from a specific inbred line, and collect DNA samples from the fathers, embryo offspring, and aged adult …

Figure 9 with 1 supplement
Some Drosophila inversions show evidence for antagonistic tradeoffs and sex-specific survival.

(A) Testing for antagonistic fitness effects on reproduction and survival (encompassing viability and longevity). Each inversion’s frequency in parents after collection (2–3 weeks from eclosion), …

Figure 9—figure supplement 1
A plot of the observed inversion frequencies in early-eclosing and late-eclosing adult offspring cohorts, compared to the embryo frequencies.

Inversion frequency changes were largely parallel between these cohorts, and no significant effects of eclosion time were identified across maternal line cross replicates.

Additional files

Supplementary file 1

Tables containing information for experimental fly counts, primers, amplicons, inversion frequency calls, selection coefficient estimates, and p-values across the comparisons presented.

(a) Counts of D. melanogaster collected from different inbred Zambian lines to generate the F2 paternal pool. (b) Counts of D. melanogaster collected or used at the different stages of the experiments. (c) Primers and amplicon sequences used in assessing inversion frequency from genomic DNA in the D. melanogaster lab experiments. Coordinates follow D. melanogaster reference genome release 5. (d) A table of fixed differences between inversions identified from the haploid Zambia genomes from the Drosophila Genome Nexus, used for inversion frequency calling. Coordinates follow D. melanogaster reference genome release 5. (e) A table of p-values calculated for non-line-combined comparisons between each pair of male vs female cohorts. (f) A table of p-values calculated for non-line-combined comparisons between each pair of early vs late eclosing cohorts. (g) A table of p-values calculated for non-line-combined comparisons between each pair of paternal vs embryo cohorts. (h) A table of p-values calculated for non-line-combined comparisons between each pair of embryo vs aged offspring cohorts.(i) A table of p-values calculated for non-line-combined tests of an increase then decrease across paternal to embryo to aged offspring sets.(j) A table of p-values calculated for non-line-combined tests of a decrease then increase across paternal to embryo to aged offspring sets.(k) A table of p-values for increase-then-decrease tests of paternal-embryo-aged offspring which have been combined across experiments of different maternal inbred line by using fishers combined p-value across maternal lines, then multiple test corrected across tested inversions and directions.(l) A table of p-values for decrease-then-increase tests of paternal-embryo-aged offspring which have been combined across experiments of different maternal inbred line by using fishers combined p-value across maternal lines, then multiple test corrected across tested inversions and directions.(m) A table of p-values for male vs female comparisons combined across experiments of different maternal inbred line by using fishers combined p-value across maternal lines, then multiple test corrected across tested inversions.(n) A table of p-values for early vs late eclosing comparisons combined across experiments of different maternal inbred line by using fishers combined p-value across maternal lines, then multiple test corrected across tested inversions.(o) A table of selection estimates generated by modeling the experimental generation as a Wright-Fisher population (p) Data on the libraries generated from experimental cohorts to estimate the inversion frequencies. Library names represent the maternal line, the cohort, the inversion chromosome arm,.the library prep, and the sequencing run. (q) Data taken by summing the read counts from duplicate libraries generated from experimental cohorts to estimate the inversion frequencies. Pool names represent the maternal line, the cohort, the inversion chromosome arm. (r) Data on the replicate libraries generated from the DNA extractions of experimental cohorts used to estimate the sample-size independent variation introduced by the library preparation and sequencing. Library names represent the source sample or line.the fly pool.the inversion.the extraction and library prep replicate. (s) Data on further replicate libraries including multiple DNA extractions of different inbred fly pools with known inversion frequency, used to estimate bias and the sample-size independent variation introduced by the library preparation and sequencing. Library names represent the source sample or line.the fly pool.the inversion.the extraction and library prep replicate.

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