Sex-limited experimental evolution drives transcriptomic divergence in a hermaphrodite
Cīrulis, Aivars LU ; Nordén, Anna K. LU ; Churcher, Allison M. ; Ramm, Steven A. ; Zadesenets, Kira S. and Abbott, Jessica K. LU
(2024)
In Genome Biology and Evolution
16(1).
- Abstract
The evolution of gonochorism from hermaphroditism is linked with the formation of sex chromosomes, as well as the evolution of sex-biased and sex-specific gene expression to allow both sexes to reach their fitness optimum. There is evidence that sexual selection drives the evolution of male-biased gene expression in particular. However, previous research in this area in animals comes from either theoretical models or comparative studies of already old sex chromosomes. We therefore investigated changes in gene expression under 3 different selection regimes for the simultaneous hermaphrodite Macrostomum lignano subjected to sex-limited experimental evolution (i.e. selection for fitness via eggs, sperm, or a control regime allowing both).... (More)
The evolution of gonochorism from hermaphroditism is linked with the formation of sex chromosomes, as well as the evolution of sex-biased and sex-specific gene expression to allow both sexes to reach their fitness optimum. There is evidence that sexual selection drives the evolution of male-biased gene expression in particular. However, previous research in this area in animals comes from either theoretical models or comparative studies of already old sex chromosomes. We therefore investigated changes in gene expression under 3 different selection regimes for the simultaneous hermaphrodite Macrostomum lignano subjected to sex-limited experimental evolution (i.e. selection for fitness via eggs, sperm, or a control regime allowing both). After 21 and 22 generations of selection for male-specific or female-specific fitness, we characterized changes in whole-organism gene expression. We found that female-selected lines had changed the most in their gene expression. Although annotation for this species is limited, gene ontology term and Kyoto Encyclopedia of Genes and Genomes pathway analyses suggest that metabolic changes (e.g. biosynthesis of amino acids and carbon metabolism) are an important adaptive component. As predicted, we found that the expression of genes previously identified as testis-biased candidates tended to be downregulated in the female-selected lines. We did not find any significant expression differences for previously identified candidates of other sex-specific organs, but this may simply reflect that few transcripts have been characterized in this way. In conclusion, our experiment suggests that changes in testis-biased gene expression are important in the early evolution of sex chromosomes and gonochorism.
(Less)
- author
- Cīrulis, Aivars
LU
; Nordén, Anna K.
LU
; Churcher, Allison M.
; Ramm, Steven A.
; Zadesenets, Kira S.
and Abbott, Jessica K.
LU
- organization
- publishing date
- 2024
- type
- Contribution to journal
- publication status
- published
- subject
- keywords
- evolution of gonochorism, experimental evolution, hermaphrodite, Macrostomum lignano, sex chromosome evolution, sex-biased gene expression, sexual selection
- in
- Genome Biology and Evolution
- volume
- 16
- issue
- 1
- article number
- evad235
- publisher
- Oxford University Press
- external identifiers
-
- pmid:38155579
- scopus:85182576924
- ISSN
- 1759-6653
- DOI
- 10.1093/gbe/evad235
- language
- English
- LU publication?
- yes
- id
- caa95991-91a0-4daa-af21-1d1b3e18419a
- date added to LUP
- 2024-02-16 12:35:41
- date last changed
- 2024-04-17 06:19:52
@article{caa95991-91a0-4daa-af21-1d1b3e18419a,
abstract = {{<p>The evolution of gonochorism from hermaphroditism is linked with the formation of sex chromosomes, as well as the evolution of sex-biased and sex-specific gene expression to allow both sexes to reach their fitness optimum. There is evidence that sexual selection drives the evolution of male-biased gene expression in particular. However, previous research in this area in animals comes from either theoretical models or comparative studies of already old sex chromosomes. We therefore investigated changes in gene expression under 3 different selection regimes for the simultaneous hermaphrodite Macrostomum lignano subjected to sex-limited experimental evolution (i.e. selection for fitness via eggs, sperm, or a control regime allowing both). After 21 and 22 generations of selection for male-specific or female-specific fitness, we characterized changes in whole-organism gene expression. We found that female-selected lines had changed the most in their gene expression. Although annotation for this species is limited, gene ontology term and Kyoto Encyclopedia of Genes and Genomes pathway analyses suggest that metabolic changes (e.g. biosynthesis of amino acids and carbon metabolism) are an important adaptive component. As predicted, we found that the expression of genes previously identified as testis-biased candidates tended to be downregulated in the female-selected lines. We did not find any significant expression differences for previously identified candidates of other sex-specific organs, but this may simply reflect that few transcripts have been characterized in this way. In conclusion, our experiment suggests that changes in testis-biased gene expression are important in the early evolution of sex chromosomes and gonochorism.</p>}},
author = {{Cīrulis, Aivars and Nordén, Anna K. and Churcher, Allison M. and Ramm, Steven A. and Zadesenets, Kira S. and Abbott, Jessica K.}},
issn = {{1759-6653}},
keywords = {{evolution of gonochorism; experimental evolution; hermaphrodite; Macrostomum lignano; sex chromosome evolution; sex-biased gene expression; sexual selection}},
language = {{eng}},
number = {{1}},
publisher = {{Oxford University Press}},
series = {{Genome Biology and Evolution}},
title = {{Sex-limited experimental evolution drives transcriptomic divergence in a hermaphrodite}},
url = {{http://dx.doi.org/10.1093/gbe/evad235}},
doi = {{10.1093/gbe/evad235}},
volume = {{16}},
year = {{2024}},
}