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Cited by 23Neuroendocrine regulation and behaviorAnimal Behavior and ReproductionNeurotransmitter Receptor Influence on Behavior

Gene expression correlates of social evolution in coral reef butterflyfishes

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Nowicki, Jessica P., Pratchett, Morgan S., Walker, Stefan P. W., Coker, Darren J., O'Connell, Lauren A.·2020·Proceedings of the Royal Society B: Biological Sciences
DOI 10.1098/rspb.2020.0239PMC PMC7329040

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Abstract

Animals display remarkable variation in social behaviour. However, outside of rodents, little is known about the neural mechanisms of social variation, and whether they are shared across species and sexes, limiting our understanding of how sociality evolves. Using coral reef butterflyfishes, we examined gene expression correlates of social variation (i.e. pair bonding versus solitary living) within and between species and sexes. In several brain regions, we quantified gene expression of receptors important for social variation in mammals: oxytocin ( OTR ), arginine vasopressin ( V1aR ), dopamine ( D1R, D2R ) and mu-opioid ( MOR ). We found that social variation across individuals of the oval butterflyfish, Chaetodon lunulatus, is linked to differences in OTR , V1aR, D1R, D2R and MOR gene expression within several forebrain regions in a sexually dimorphic manner. However, this contrasted with social variation among six species representing a single evolutionary transition from pair-bonded to solitary living. Here, OTR expression within the supracommissural part of the ventral telencephalon was higher in pair-bonded than solitary species, specifically in males. These results contribute to the emerging idea that nonapeptide, dopamine and opioid signalling is a central theme to the evolution of sociality across individuals, although the precise mechanism may be flexible across sexes and species.

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  • Collectively, studies in zebra finches, butterflyfishes, and other species emphasize the significance of the interplay between OXT and DA and their combined impact on pair bonding, extending beyond the context of humans and rodents.

    “Collectively, these studies (Anderson et al., 2023; Day et al., 2019; Nowicki et al., 2020) emphasize the significance of the interplay between OXT and DA and their combined impact on pair bonding, extending beyond the context of humans and rodents.”

    From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Nowicki et al., 2020

    The Abstract and Conclusion link oxytocin- and dopamine-receptor expression to pair-bonded versus solitary living in butterflyfishes, supporting the claim’s extension beyond rodents and humans. But the Results (Pair-bonded versus solitary Chaetodon species) report no dopamine-receptor differences between pair-bonded and solitary species, and the paper does not test an OXT–DA interaction or establish their combined impact on pair bonding. Page numbers are not provided in our copy. (LLM, conf=0.85)

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  • Individual differences in sociality were associated with OXTR and D1R expression in the dorsal portion of the ventral telencephalon, the mammalian homologue of the NAc, in coral reef butterflyfishes.

    “The study found that individual differences in sociality were associated with OXTR and D1R expression in the dorsal portion of the ventral telencephalon, the mammalian homologue of the NAc.”

    From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Nowicki et al., 2020

    The Results (Pair-bonded versus solitary Chaetodon lunulatus; page unavailable) report significant differences in Vd D1R expression between solitary and pair-bonded individuals of both sexes. Vd OTR (OXTR) expression showed a similar trend only in females, but it was not statistically significant (p = 0.07). The Discussion identifies Vd as a putative mammalian nucleus accumbens homologue, so the claim captures the region and receptors but overstates the OXTR finding and omits its sex-specific qualification. (LLM, conf=0.88)

    Experimental — accuracy not yet measured

  • There were no major changes in OXTR as well as D1R and D2R expression in the VTA in coral reef butterflyfishes.

    “However, there were no major changes in OXTR as well as D1 receptor (D1R) and D2 receptor (D2R) expression in the VTA.”

    From Convergence of oxytocin and dopamine signalling in neuronal circuits: Insights into the neurobiology of social interactions across species (2024) · cites this paper as Nowicki et al., 2020

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Research works printed but not linked: 40

  1. [1]Goodson JL 2013 Deconstructing sociality, social evolution and relevant nonapeptide functions. Psychoneuroendocrinology 38, 465– 478. (10.1016/j.psyneuen.2012.12.005) 23290368 · DOI · Paper page
  2. [2]McGraw L, Székely T, Young LJ 2010 Pair bonds and parental behaviour. In Social behaviour: genes, ecology and evolution (eds Székely T, Moore AJ, Komdeur J), pp. 271– 301. Cambridge, UK: Cambridge University Press.
  3. [3]Nowicki JP, O'Connell LA, Cowman PF, Walker SPW, Coker DJ, Pratchett MS 2018 Variation in social systems within Chaetodon butterflyfishes, with special reference to pair bonding. PLoS ONE 13, e0194465 (10.1371/journal.pone.0194465) 29641529 PMC5894994 · DOI
  4. [4]Zheng D-J, Larsson B, Phelps SM, Ophir AG 2013 Female alternative mating tactics, reproductive success and nonapeptide receptor expression in the social decision-making network. Behav. Brain Res. 246, 139– 147. (10.1016/j.bbr.2013.02.024) 23500897 PMC3633648 · DOI
  5. [5]Firth JA, Cole EF, Ioannou CC, Quinn JL, Aplin LM, Culina A, McMahon K, Sheldon BC 2018 Personality shapes pair bonding in a wild bird social system. Nat. Ecol. Evol. 2, 1696– 1699. (10.1038/s41559-018-0670-8) 30275466 PMC6217997 · DOI
  6. [6]Walum H et al 2008 Genetic variation in the vasopressin receptor 1a gene (AVPR1A) associates with pair-bonding behavior in humans. Proc. Natl Acad. Sci. USA 105, 14 153– 14 156. (10.1073/pnas.0803081105) PMC2533683 18765804 · DOI · Paper page
  7. [8]Freeman SM, Young L 2013 Oxytocin, vasopressin, and the evolution of mating systems in mammals. In Oxytocin, vasopressin and related peptides in the regulation of behavior (eds Choleris E, Pfaff DW, Kavaliers M), pp. 128– 144. Cambridge, UK: Cambridge University Press.
  8. [9]Shapiro LE, Insel TR 1992 Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Ann. NY Acad. Sci. 652, 448– 451. (10.1111/j.1749-6632.1992.tb34380.x) 1320837 · DOI · Paper page
  9. [10]O'Connell LA, Hofmann HA 2012 Evolution of a vertebrate social decision-making network. Science 336, 1154– 1157. (10.1126/science.1218889) 22654056 · DOI · Paper page
  10. [11]O'Connell LA, Hofmann HA 2011 The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J. Comp. Neurol. 519, 3599– 3639. (10.1002/cne.22735) 21800319 · DOI · Paper page
  11. [12]Carter CS, Cushing BS 2004 Proximate mechanisms regulating sociality and social monogamy, in the context of evolution. In The origins and nature of sociality (eds Sussman RW, Chapman AR), pp. 99– 121. Hillsdale, NJ: Transaction Publishers.
  12. [13]Ondrasek NR 2016 Emerging frontiers in social neuroendocrinology and the study of nonapeptides. Ethology 122, 443– 455. (10.1111/eth.12493) · DOI
  13. [14]Fischer EK, Nowicki J, O'Connell LA 2019 Evolution of affiliation: patterns of convergence from genomes to behavior. Phil. Trans. R. Soc. B 374, 20180242 (10.1098/rstb.2018.0242) 31154971 PMC6560274 · DOI
  14. [15]Dewan AK, Ramey ML, Tricas TC 2011 Arginine vasotocin neuronal phenotypes, telencephalic fiber varicosities, and social behavior in butterflyfishes (Chaetodontidae): potential similarities to birds and mammals. Horm. Behav. 59, 56– 66. (10.1016/j.yhbeh.2010.10.002) 20950619 · DOI
  15. [16]Dewan AK, Tricas TC 2011 Arginine vasotocin neuronal phenotypes and their relationship to aggressive behavior in the territorial monogamous multiband butterflyfish, Chaetodon multicinctus. Brain Res. 1401, 74– 84. (10.1016/j.brainres.2011.05.029) 21676381 · DOI
  16. [17]Cowman PF, Bellwood DR 2011 Coral reefs as drivers of cladogenesis: expanding coral reefs, cryptic extinction events, and the development of biodiversity hotspots. J. Evol. Biol. 24, 2543– 2562. (10.1111/j.1420-9101.2011.02391.x) 21985176 · DOI
  17. [18]Bellwood DR, Pratchett MS 2013 The origins and diversification of coral reef butterflyfishes. In Biology of butterflyfishes (eds Pratchett MS, Berumen ML, Kapoor BG), pp. 1– 18. Boca Raton, FL: CRC Press.
  18. [19]Nowicki JP, Walker SPW, Coker DJ, Hoey AS, Nicolet KJ, Pratchett MS 2018 Pair bond endurance promotes cooperative food defense and inhibits conflict in coral reef butterflyfish. Sci. Rep. 8, 6295 (10.1038/s41598-018-24412-0) 29674741 PMC5908845 · DOI
  19. [20]Fricke HW 1986 Pair swimming and mutual partner guarding in monogamous butterflyfish (pisces, chaetodontidae): a joint advertisement for territory. Ethology 73, 307– 333. (10.1111/j.1439-0310.1986.tb00812.x) · DOI
  20. [21]Pratchett MS, Pradjakusuma OA, Jones GP 2006 Is there a reproductive basis to solitary living versus pair-formation in coral reef fishes? Coral Reefs 25, 85– 92. (10.1007/s00338-005-0081-6) · DOI
  21. [23]Pratchett MS, Berumen ML, Kapoor BG 2013 Biology of butterflyfishes. Boca Raton, FL: CRC Press.
  22. [24]Roberts CM, Ormond FG 1992 Butterflyfish social behaviour, with special reference to the incidence of territoriality: a review. Environ. Biol. Fishes 34, 79– 93. (10.1007/BF00004786) · DOI
  23. [25]Bauchot R, Ridet JM, Bauchot ML 1989 The brain organization of butterflyfishes. Environ. Biol. Fishes 25, 204– 219. (10.1007/BF00002213) · DOI
  24. [26]Dewan AK, Tricas TC 2014 Cytoarchitecture of the telencephalon in the coral reef multiband butterflyfish (Chaetodon multicinctus: Perciformes). Brain Behav. Evol. 84, 31– 50. (10.1159/000363124) 25138693 · DOI
  25. [27]Matz MV, Wright RM, Scott JG 2013 No control genes required: Bayesian analysis of qRT-PCR data. PLoS ONE 8, e71448 (10.1371/journal.pone.0071448) 23977043 PMC3747227 · DOI
  26. [28]Ophir AG, Wolff JO, Phelps SM 2008 Variation in neural V1aR predicts sexual fidelity and space use among male prairie voles in semi-natural settings. Proc. Natl Acad. Sci. USA 105, 1249– 1254. (10.1073/pnas.0709116105) 18212120 PMC2234124 · DOI
  27. [30]Insel TR, Wang ZX, Ferris CF 1994 Patterns of brain vasopressin receptor distribution associated with social-organization in microtine rodents. J. Neurosci. 14, 5381– 5392. (10.1523/JNEUROSCI.14-09-05381.1994) 8083743 PMC6577077 · DOI · Paper page
  28. [31]Insel TR, Shapiro LE 1992 Oxytocin receptor distribution reflects social organization in monogamous and polygamous voles. Proc. Natl Acad. Sci. USA 89, 5981– 5985. (10.1073/pnas.89.13.5981) 1321430 PMC402122 · DOI · Paper page
  29. [33]Inoue K, Burkett JP, Young LJ 2013 Neuroanatomical distribution of μ-opioid receptor mRNA and binding in monogamous prairie voles (Microtus ochrogaster) and non-monogamous meadow voles (Microtus pennsylvanicus). Neuroscience 244, 122– 133. (10.1016/j.neuroscience.2013.03.035) 23537838 PMC4327842 · DOI
  30. [34]Bester-Meredith JK, Young LJ, Marler CA 1999 Species differences in paternal behavior and aggression in peromyscus and their associations with vasopressin immunoreactivity and receptors. Horm. Behav. 36, 25– 38. (10.1006/hbeh.1999.1522) 10433884 · DOI
  31. [35]Turner LM, Young AR, Rompler H, Schoneberg T, Phelps SM, Hoekstra HE 2010 Monogamy evolves through multiple mechanisms: evidence from V1aR in deer mice. Mol. Biol. Evol. 27, 1269– 1278. (10.1093/molbev/msq013) 20097658 · DOI
  32. [36]Renn SCP, Machado HE, Duftner N, Sessa AK, Harris RM, Hofmann HA 2018 Gene expression signatures of mating system evolution. Genome 61, 287– 297. (10.1139/gen-2017-0075) 28945978 · DOI
  33. [37]Young RL et al 2019 Conserved transcriptomic profiles underpin monogamy across vertebrates. Proc. Natl Acad. Sci. USA 116, 1331– 1336. (10.1073/pnas.1813775116) 30617061 PMC6347671 · DOI
  34. [38]Goodson JL, Evans AK, Wang Y 2006 Neuropeptide binding reflects convergent and divergent evolution in species-typical group sizes. Horm. Behav. 50, 223– 236. (10.1016/j.yhbeh.2006.03.005) 16643915 PMC2570780 · DOI
  35. [39]Kirkpatrick B, Carter CS, Newman SW, Insel TR 1994 Axon-sparing lesions of the medial nucleus of the amygdala decrease affiliative behaviors in the prairie vole (Microtus ochrogaster): behavioral and anatomical specificity. Behav. Neurosci. 108, 501 (10.1037/0735-7044.108.3.501) 7917044 · DOI
  36. [40]Ferguson JN, Young LJ, Hearn EF, Matzuk MM, Insel TR, Winslow JT 2000 Social amnesia in mice lacking the oxytocin gene. Nat. Genet. 25, 284– 288. (10.1038/77040) 10888874 · DOI · Paper page
  37. [41]Ferguson JN, Aldag JM, Insel TR, Young LJ 2001 Oxytocin in the medial amygdala is essential for social recognition in the mouse. J. Neurosci. 21, 8278– 8285. (10.1523/JNEUROSCI.21-20-08278.2001) 11588199 PMC6763861 · DOI · Paper page
  38. [42]Ohya T, Hayashi S 2006 Vasotocin/isotocin-immunoreactive neurons in the medaka fish brain are sexually dimorphic and their numbers decrease after spawning in the female. Zool. Sci. 23, 23– 29. (10.2108/zsj.23.23) 16547402 · DOI
  39. [43]Kawabata Y, Hiraki T, Takeuchi A, Okubo K 2012 Sex differences in the expression of vasotocin/isotocin, gonadotropin-releasing hormone, and tyrosine and tryptophan hydroxylase family genes in the medaka brain. Neuroscience 218, 65– 77. (10.1016/j.neuroscience.2012.05.021) 22609934 · DOI
  40. [44]Nowicki JP, Pratchett MS, Walker SPW, Coker DJ, O'Connell LA 2020 Data from: Gene expression correlates of social evolution in coral reef butterflyfishes. Dryad Digital Repository. (10.5061/dryad.zcrjdfn7h) PMC7329040 32576103 · DOI

Cited by

Sorted by citations

Authors
Nowicki, J. P., Pratchett, M. S., Walker, S. P. W., Coker, D. J., & O'Connell, L. A.
Affiliations
  • ARC Centre of Excellence for Coral Reef Studies (AU)
  • Department of Biology, Stanford University, 371 Jane Stanford Way, Stanford, CA 94305, USA
ORCID
Venue
Proceedings of the Royal Society B: Biological Sciences
Publisher
The Royal Society
Published
2020-06-24
Volume
287
Issue
1929
Pages
20200239
ISSN
  • 0080-4649 (ISSN-L)
  • 0962-8452
  • 1471-2954
DOI
10.1098/rspb.2020.0239
PMC
PMC7329040
OpenAlex
W3037229575
Cited by
23
References
3
Citations by year
2025: 6 · 2024: 4 · 2023: 4 · 2022: 2 · 2021: 4 · 2020: 3
FWCI
3.55
Type
journal article
Language
en
Open access
Licence
Locations
  • Proceedings of the Royal Society B Biological Sciences (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • King Abdullah University of Science and Technology Repository (King Abdullah University of Science and Technology) (submittedVersion, other-oa)
Funders
  • NSF EDEN Research Travel Award (0955517)
  • Harvard Bauer Fellowship
  • L'Oreal For Women in Science
  • ARC Centre of Excellence for Coral Reef Studies (CEO561435)
  • New York Stem Cell Foundation
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
  • Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Neurotransmitter Receptor Influence on Behavior
Keywords
social evolution, sociality, pair bonding, living alone, gene expression, oxytocin receptor, dopamine receptors, mu-opioid receptor, forebrain, telencephalon, sexual dimorphism, social behavior
MeSH terms
Animals, Perciformes, Social Behavior, Telencephalon, Vasopressins, Gene Expression, Coral Reefs

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