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Functional convergence of genomic and transcriptomic architecture underlies schooling behaviour in a live-bearing fish

Corral-Lopez, Alberto ; Bloch, Natasha I. ; van der Bijl, Wouter ; Cortazar-Chinarro, Maria LU ; Szorkovszky, Alexander ; Kotrschal, Alexander ; Darolti, Iulia ; Buechel, Severine D. ; Romenskyy, Maksym and Kolm, Niclas , et al. (2024) In Nature Ecology and Evolution 8(1). p.98-110
Abstract

The organization and coordination of fish schools provide a valuable model to investigate the genetic architecture of affiliative behaviours and dissect the mechanisms underlying social behaviours and personalities. Here we used replicate guppy selection lines that vary in schooling propensity and combine quantitative genetics with genomic and transcriptomic analyses to investigate the genetic basis of sociability phenotypes. We show that consistent with findings in collective motion patterns, experimental evolution of schooling propensity increased the sociability of female, but not male, guppies when swimming with unfamiliar conspecifics. This finding highlights a relevant link between coordinated motion and sociability for species... (More)

The organization and coordination of fish schools provide a valuable model to investigate the genetic architecture of affiliative behaviours and dissect the mechanisms underlying social behaviours and personalities. Here we used replicate guppy selection lines that vary in schooling propensity and combine quantitative genetics with genomic and transcriptomic analyses to investigate the genetic basis of sociability phenotypes. We show that consistent with findings in collective motion patterns, experimental evolution of schooling propensity increased the sociability of female, but not male, guppies when swimming with unfamiliar conspecifics. This finding highlights a relevant link between coordinated motion and sociability for species forming fission–fusion societies in which both group size and the type of social interactions are dynamic across space and time. We further show that alignment and attraction, the two major traits forming the sociability personality axis in this species, showed heritability estimates at the upper end of the range previously described for social behaviours, with important variation across sexes. The results from both Pool-seq and RNA-seq data indicated that genes involved in neuron migration and synaptic function were instrumental in the evolution of sociability, highlighting a crucial role of glutamatergic synaptic function and calcium-dependent signalling processes in the evolution of schooling.

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organization
publishing date
type
Contribution to journal
publication status
published
subject
in
Nature Ecology and Evolution
volume
8
issue
1
pages
13 pages
publisher
Nature Publishing Group
external identifiers
  • pmid:37985898
  • scopus:85173094570
ISSN
2397-334X
DOI
10.1038/s41559-023-02249-9
language
English
LU publication?
yes
id
064086d5-b0b6-4d25-bbce-834cd33c124b
date added to LUP
2024-01-15 13:03:40
date last changed
2024-04-15 23:40:21
@article{064086d5-b0b6-4d25-bbce-834cd33c124b,
  abstract     = {{<p>The organization and coordination of fish schools provide a valuable model to investigate the genetic architecture of affiliative behaviours and dissect the mechanisms underlying social behaviours and personalities. Here we used replicate guppy selection lines that vary in schooling propensity and combine quantitative genetics with genomic and transcriptomic analyses to investigate the genetic basis of sociability phenotypes. We show that consistent with findings in collective motion patterns, experimental evolution of schooling propensity increased the sociability of female, but not male, guppies when swimming with unfamiliar conspecifics. This finding highlights a relevant link between coordinated motion and sociability for species forming fission–fusion societies in which both group size and the type of social interactions are dynamic across space and time. We further show that alignment and attraction, the two major traits forming the sociability personality axis in this species, showed heritability estimates at the upper end of the range previously described for social behaviours, with important variation across sexes. The results from both Pool-seq and RNA-seq data indicated that genes involved in neuron migration and synaptic function were instrumental in the evolution of sociability, highlighting a crucial role of glutamatergic synaptic function and calcium-dependent signalling processes in the evolution of schooling.</p>}},
  author       = {{Corral-Lopez, Alberto and Bloch, Natasha I. and van der Bijl, Wouter and Cortazar-Chinarro, Maria and Szorkovszky, Alexander and Kotrschal, Alexander and Darolti, Iulia and Buechel, Severine D. and Romenskyy, Maksym and Kolm, Niclas and Mank, Judith E.}},
  issn         = {{2397-334X}},
  language     = {{eng}},
  number       = {{1}},
  pages        = {{98--110}},
  publisher    = {{Nature Publishing Group}},
  series       = {{Nature Ecology and Evolution}},
  title        = {{Functional convergence of genomic and transcriptomic architecture underlies schooling behaviour in a live-bearing fish}},
  url          = {{http://dx.doi.org/10.1038/s41559-023-02249-9}},
  doi          = {{10.1038/s41559-023-02249-9}},
  volume       = {{8}},
  year         = {{2024}},
}