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Gene Expression Modification by an Autosomal Inversion Associated With Three Male Mating Morphs.

Jasmine L Loveland1, David B Lank2, Clemens Küpper1

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Summary

A large autosomal inversion in ruff birds creates three male morphs. This inversion impacts gene expression, particularly near breakpoints, and allows morphs to be distinguished by their overall gene expression profiles.

Keywords:
CENPNHSD17B2Philomachus pugnaxSDR42E1alternative reproduction strategiesaromatasechromosomal inversionsteroidogenic pathway

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Area of Science:

  • Evolutionary genetics
  • Genomics
  • Animal behavior

Background:

  • Chromosomal inversions are key drivers of phenotypic diversity.
  • In ruff birds (Philomachus pugnax), a 4.5 Mb autosomal inversion determines three distinct male reproductive morphs: Independents, Satellites, and Faeders.
  • The impact of this stable inversion polymorphism on gene expression during the lekking season is not fully understood.

Purpose of the Study:

  • To investigate how the stable inversion polymorphism affects gene expression in male ruffs during the lekking season.
  • To determine if gene expression is altered by disruptions at inversion breakpoints or by suppressed recombination.
  • To analyze allelic imbalance and gene expression patterns across different tissues and morphs.

Main Methods:

  • Quantitative PCR was used to measure the expression of 11 candidate inversion genes in liver, adrenal glands, and gonads.
  • Allelic imbalance was tested in four inversion genes across 12 males representing all three morphs.
  • Linear discriminant analysis (LDA) was applied to gene expression data from 25 males (13 Independents, 7 Satellites, 5 Faeders) to differentiate morphs.

Main Results:

  • The breakpoint gene CENPN showed dosage-dependent expression, with Satellites and Faeders exhibiting twofold higher expression in non-inverted regions compared to inverted regions.
  • Allelic imbalance was observed in inversion genes when analyzed with allele-specific primers.
  • While individual gene expression did not clearly differentiate morphs, LDA successfully distinguished all three morphs based on overall gene expression patterns, irrespective of gene location.

Conclusions:

  • The stable autosomal inversion in ruffs significantly influences gene expression, particularly affecting genes near breakpoints and leading to allelic imbalance.
  • Gene expression profiles provide a robust method for distinguishing between the three male morphs, highlighting the complex effects of structural variants.
  • The findings suggest that chromosomal inversions can lead to widespread and intricate changes in gene expression, contributing to evolutionary diversification.