Research Paper Volume 16, Issue 18 pp 12443—12472

Single housing of juveniles accelerates early-stage growth but extends adult lifespan in African turquoise killifish

Chika Takahashi1, , Emiko Okabe1, , Masanori Nono1, , Saya Kishimoto1, , Hideaki Matsui2, , Tohru Ishitani3, , Takuya Yamamoto4,5,6, , Masaharu Uno1, , Eisuke Nishida1, ,

  • 1 Laboratory for Molecular Biology of Aging, RIKEN Center for Biosystems Dynamics Research (BDR), Hyogo, Japan
  • 2 Department of Neuroscience of Disease, Brain Research Institute, Niigata University, Niigata, Japan
  • 3 Department of Homeostatic Regulation, Division of Cellular and Molecular Biology, Research Institute for Microbial Diseases, Osaka University, Osaka, Japan
  • 4 Center for iPS Cell Research and Application (CiRA), Kyoto University, Kyoto, Japan
  • 5 Institute for the Advanced Study of Human Biology (WPI-ASHBi), Kyoto University, Kyoto, Japan
  • 6 Medical-risk Avoidance based on iPS Cells Team, RIKEN Center for Advanced Intelligence Project (AIP), Kyoto, Japan

Received: April 3, 2024       Accepted: August 3, 2024       Published: September 16, 2024      

https://doi.org/10.18632/aging.206111
How to Cite

Copyright: © 2024 Takahashi et al. This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Abstract

Within the same species, individuals exhibiting faster growth tend to have shorter lifespans, even if their fast growth arises from early-life pharmacological interventions. However, in vertebrates, the impact of the early-life environment on the growth rate and lifespan has not been fully elucidated. In this study, by utilizing the short-lived African turquoise killifish, which is suitable for a comprehensive life-stage analysis in a brief timeframe, we explored the effects of housing density during the juvenile stage on holistic life traits. As a result, we found that lower housing densities resulted in faster growth, but led to longer adult lifespan, which was contrary to the common notion. Furthermore, the single-housed adult fish displayed a longer egg-laying period than did their group-housed counterparts. Our transcriptome analysis also demonstrated that, in terms of internal transcriptional programs, the life stage progression and aging process of single-housed fish were slower than those of group-housed fish. Collectively, our results suggest that sharing housing with others in early life might influence whole-life attributes, potentially leading to specific life history traits beyond the typical relationship between the growth rate and lifespan.

Abbreviations

wph: weeks posthatching; dph: days posthatching; TPM: transcripts per million; PCA: principal component analysis; GO: gene ontology; DEG: differentially expressed gene; DOHaD: developmental origins of health and disease; piwil1: piwi like RNA-mediated gene silencing 1; dazl: deleted in azoospermia like; sycp3: synaptonemal complex protein 3; odf3b: outer dense fiber of sperm tails 3B; tdrd1: tudor domain containing 1; tdrd7a: tudor domain containing 7a; tdrd6: tudor domain containing 6; tdrd15: tudor domain containing 15; dctn2: dynactin 2; pld6: phospholipase D family, member 6; buc: bucky ball; pum1: pumilio RNA-binding family member 1; tdrkn: tudor and KH domain containing; figla: folliculogenesis specific bHLH transcription factor; ythdf2: YTH N6-methyladenosine RNA binding protein F2; lhcgr: luteinizing hormone/choriogonadotropin receptor; cyp19a1a: cytochrome P450, family 19, subfamily A, polypeptide 1a; pla2g4ab: phospholipase A2, group IVAb; fshr: follicle stimulating hormone receptor; ythdf3: YTH N6-methyladenosine RNA binding protein F3; pgrmc1: progesterone receptor membrane component 1; il-8: interleukin 8; tfa: transferrin-a.