Evolution of sex and mating loci: an expanded view from Volvocine algae

Abstract

Sexual reproduction in Volvocine algae coevolved with the acquisition of multicellularity. Unicellular genera such as Chlamydomonas and small colonial genera from this group have classical mating types with equal-sized gametes, while larger multicellular genera such as Volvox have differentiated males and females that produce sperm and eggs respectively. Newly available sequence from the Volvox and Chlamydomonas genomes and mating loci open up the potential to investigate how sex-determining regions co-evolve with major changes in development and sexual reproduction. The expanded size and sequence divergence between the male and female haplotypes of the Volvox mating locus (MT) not only provide insights into how the colonial Volvocine algae might have evolved sexual dimorphism, but also raise questions about why the putative ancestral-like MT locus in Chlamydomonas shows less divergence between haplotypes than expected.

Figure 1

A. Two Chlamydomonas cells. Scale bar is 10 μM. B. Vegetative Volvox spheroid. C. Sexual female Volvox spheroid. D. Sexual Male Volvox spheroid. Scale bar is 50 μM for panels B–D. E. Schematic of Chlamydomonas life cycle. Left side depicts the vegetative reproductive cycle of growth, and division by multiple fission. Right side depicts mating, diploid MT+/MT− zygotic spore formation, meiosis and hatching to produce four haploid progeny. F. Schematic of the Volvox life cycle. Left side depicts key stages in the vegetative reproductive cycle. Starting in the upper right are a mature spheroid, cleavage stage embryo, pre-inversion embryo, inverted juvenile, expanding juvenile, and hatching stage. Right side depicts the sexual cycle. Pre-cleavage gonidia from males and females undergo modified development to produce sperm packet bearing male spheroids and egg bearing female spheroids. Sperm travel as a packet, attach to a female, dissociate, enter, and fertilize eggs to form a diploid MTF/MTM zygotic spore. Meiosis and germination produce a single haploid vegetative progeny (either male or female) and three polar bodies.

Figure 2

Schematic of the Chlamydomonas and Volvox mating type chromosomes and mating loci. The rearranged (R) domain and its relative location on each chromosome is labeled. Above and below the chromosomal schematics are expanded versions of MT from each species with the R domain for each haplotype shown in red or blue and genes overlaid in gray. EZY2/OTU2 are in a tandem repeat region. Several sex-limited genes are shown for each species, with vegetative expression depicted by a green dot, sexual expression by a red dot, and zygotic expression by a black dot [18,19**].

Figure 3

A. Model for expansion of Volvox MT. The R domain is red or blue and the autosomal region is green. SD represents a sex determining gene, and A and B are flanking genes. Autosomal inversions adjacent to the existing R domain will block recombination and allow differentiation of the formerly autosomal A/a and B/b loci in linkage with mating haplotype. Sexually antagonistic alleles B and b (shaded red and blue) can be fixed if they contribute to fitness of their respective mating types [19**]. B. Expected divergence patterns for MT if no recombination occurred in either the Chlamydomonas or Volvox lineages. Light red and blue represent less diverged regions while darker red and blue represent more diverged regions. More recently acquired regions of Volvox MT should be less diverged, while the older regions should have divergence similar to that seen in Chlamydomonas. This divergence pattern is not observed (see text). C. Mating type resetting can occur if a mid mutation and FUS1 gene end up on the same chromosome to generate a neo-MT+ haplotype that is highly similar to MT−. D. Mating type sequence homogenization can occur through gene conversion between MT+ and MT− shared genes.