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Evolution of the reproductive interactome and the origins of postmating–prezygotic reproductive divergence

ABSTRACT: Reproductive proteins evolve rapidly, which is predicted to cause postmating-prezygotic (PMPZ) reproductive isolation between divergent populations. While most previous studies have focused on protein sequence divergence as a likely driver of PMPZ incompatibilities, reproductive proteomes may also diverge compositionally and/or quantitatively. Here, we characterize extensive protein sequence, compositional, and quantitative divergence of male and female reproductive proteomes in two species exhibiting strong PMPZ isolation (D. mojavensis and D. arizonae). We further demonstrate that three divergent male seminal fluid proteins affect the size of the insemination reaction mass and/or fertilization success in D. arizonae. Using quantitative data and protein-protein interaction modeling of proteases and protease inhibitors, we predict the relative importance of protein sequence divergence, compositional changes, and quantitative divergence to the evolution of PMPZ incompatibilities between the species. We find that predicted interspecies protein incompatibilities arise from proteome compositional changes rather than protein sequence divergence, at least for the subset of the interactome that we tested. Furthermore, extensive quantitative divergence, particularly for proteases and inhibitors, suggests pervasive stoichiometric mismatches in heterospecific matings. Altogether, our findings provide novel insights into how the reproductive interactome diverges, and the consequences of this divergence for the evolution of PMPZ reproductive isolation.

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ORGANISM(S): Drosophila Mojavensis Mojavensis Drosophila Arizonae

TISSUE(S): Female Reproductive System, Sperm, Diploid Cell

SUBMITTER: Luciano Matzkin

LAB HEAD: Luciano Matzkin

PROVIDER: PXD065290 | Pride | 2026-04-02

REPOSITORIES: Pride

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Project description:Genetic analyses of speciation have focused nearly exclusively on retrospective analyses of reproductive isolation between highly divergent species. Yet, a full understanding of the speciation process must encompass analysis of the consequences of genomic divergence in young lineages still capable of exchanging genes under natural conditions. The accumulation of conditionally neutral genetic variation may lead to the evolution of divergent gene networks. In a hybrid background, such mutations may no longer compensate one another, resulting in the appearance of selectively disadvantageous traits, including disruption of gene expression regulation. Here, we documented genome-wide patterns of gene expression divergence between young lineages of normal and dwarf lake whitefish and their backcross hybrids for which strong, yet incomplete post-zygotic isolation barriers exist. A significant proportion (33%) of backcross hybrids showed developmental abnormalities not seen in parental forms and eventually leading to death. While the transcriptome of parental forms was nearly identical during embryonic development, suggesting a role for stabilizing selection, all hybrids displayed strongly divergent patterns of gene expression. By comparing healthy, surviving hybrids against moribund ones, we observed that over 2000 genes were misregulated in these abnormal embryos. In particular, misregulation was significantly biased towards essential developmental genes which were strongly underexpressed. Furthermore, genes previously documented to be highly transgressive (exaggerated inter-individual variance) were almost invariably underexpressed in hybrids. Our results thus clearly showed a transcriptome-wide signature of hybrid breakdown in young, incipient species and demonstrated a persuasive link between misexpression of essential developmental genes and post zygotic isolation. Samples of dwarf, normal, backcross-healthy and backcross-moribund were hybridized in a loop design, involving eight biological replicates for the backcross-healthy and backcross-moribund comparison and six for the others. Dye swap was performed between each replicate. As a result, we obtained a final set of 32 microarray slides.

			Action	DRS
	ARI-sperm.raw	Raw
	ARIcat10genename.fasta	Fasta
	MOV-sperm.raw	Raw
	MOVcat10genename.fasta	Fasta
	SILAC-SFP-CCE20200904-rep1-hfx1.raw	Raw

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Evolution of the reproductive interactome and the origins of postmating–prezygotic reproductive divergence

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