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Evolution of Sexes from an Ancestral Mating-Type Specification Pathway

2014/07/08 by Sa Geng, Peter De Hoff, James Umen · 1 citation
Energy · Earth and Planetary Sciences · Agricultural and Biological Sciences · #Algal biology and biofuel production #Marine and coastal plant biology #Biocrusts and Microbial Ecology #Biology #Gamete #Mating type #Genetics #Locus (genetics) #Mating #Gene #RNA interference #Meiosis #Sperm #Evolutionary biology #Sexual dimorphism #Zoology #RNA

paper · pdf · doi:10.1371/journal.pbio.1001904

openalex publication_date 2014/07/08 · openalex created_date 2025/10/10 · openalex updated_date 2026/08/01

Abstract

Male and female sexes have evolved repeatedly in eukaryotes but the origins of dimorphic sexes and their relationship to mating types in unicellular species are not understood. Volvocine algae include isogamous species such as Chlamydomonas reinhardtii, with two equal-sized mating types, and oogamous multicellular species such as Volvox carteri with sperm-producing males and egg-producing females. Theoretical work predicts genetic linkage of a gamete cell-size regulatory gene(s) to an ancestral mating-type locus as a possible step in the evolution of dimorphic gametes, but this idea has not been tested. Here we show that, contrary to predictions, a single conserved mating locus (MT) gene in volvocine algae-MID, which encodes a RWP-RK domain transcription factor-evolved from its ancestral role in C. reinhardtii as a mating-type specifier, to become a determinant of sperm and egg development in V. carteri. Transgenic female V. carteri expressing male MID produced functional sperm packets during sexual development. Transgenic male V. carteri with RNA interference (RNAi)-mediated knockdowns of VcMID produced functional eggs, or self-fertile hermaphrodites. Post-transcriptional controls were found to regulate cell-type-limited expression and nuclear localization of VcMid protein that restricted its activity to nuclei of developing male germ cells and sperm. Crosses with sex-reversed strains uncoupled sex determination from sex chromosome identity and revealed gender-specific roles for male and female mating locus genes in sexual development, gamete fitness and reproductive success. Our data show genetic continuity between the mating-type specification and sex determination pathways of volvocine algae, and reveal evidence for gender-specific adaptations in the male and female mating locus haplotypes of Volvox. These findings will enable a deeper understanding of how a master regulator of mating-type determination in an ancestral unicellular species was reprogrammed to control sexually dimorphic gamete development in a multicellular descendant.

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