A postmeiotically bifurcated roadmap of honeybee spermatogenesis marked by phylogenetically restricted genes

PLoS Genet. 2023 Dec 4;19(12):e1011081. doi: 10.1371/journal.pgen.1011081. eCollection 2023 Dec.

Abstract

Haploid males of hymenopteran species produce gametes through an abortive meiosis I followed by meiosis II that can either be symmetric or asymmetric in different species. Thus, one spermatocyte could give rise to two spermatids with either equal or unequal amounts of cytoplasm. It is currently unknown what molecular features accompany these postmeiotic sperm cells especially in species with asymmetric meiosis II such as bees. Here we present testis single-cell RNA sequencing datasets from the honeybee (Apis mellifera) drones of 3 and 14 days after emergence (3d and 14d). We show that, while 3d testes exhibit active, ongoing spermatogenesis, 14d testes only have late-stage spermatids. We identify a postmeiotic bifurcation in the transcriptional roadmap during spermatogenesis, with cells progressing toward the annotated spermatids (SPT) and small spermatids (sSPT), respectively. Despite an overall similarity in their transcriptomic profiles, sSPTs express the fewest genes and the least RNA content among all the sperm cell types. Intriguingly, sSPTs exhibit a relatively high expression level for Hymenoptera-restricted genes and a high mutation load, suggesting that the special meiosis II during spermatogenesis in the honeybee is accompanied by phylogenetically young gene activities.

MeSH terms

  • Animals
  • Bees / genetics
  • Male
  • Meiosis / genetics
  • Semen*
  • Spermatids / metabolism
  • Spermatocytes / metabolism
  • Spermatogenesis* / genetics
  • Testis

Grants and funding

FH was supported by two National Key R&D Program of China grants (2018YFA0800102 and 2021YFC2700403) and a National Natural Science Foundation of China grant (31871249). JM was supported by a National Natural Science Foundation of China grant (31871452). JH was supported by a National Key R&D Program of China grant (2022YFD1600205), the China Agriculture Research System-Bee (NYCYTX-44-KXJ5) and the Agricultural Science and Technology Innovation Program Chinese Academy of Agricultural Sciences (CAAS-ASTIP-2023-IAR). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.