Abstract
Author SummarySexual differentiation in eukaryotes is manifested in two fundamentally different ways. Unicellular species may have mating types where gametes are morphologically identical but can only mate with those expressing a different mating type than their own, while multicellular species such as plants and animals have male and female sexes or separate reproductive structures that produce sperm and eggs. The relationship between mating types and sexes and whether or how an ancestral mating-type system could have evolved into a sexually dimorphic system are unknown. In this study we investigated sex determination in the multicellular green alga Volvox carteri, a species with genetic sex determination; we established the relationship of V. carteri sexes to the mating types of its unicellular relative, Chlamydomonas reinhardtii. Theoretical work has suggested that sexual dimorphism could be acquired by linkage of gamete size-regulatory genes to an ancestral mating-type locus. Instead, we found that a single ancestral mating locus gene, MID, evolved from its role in determining mating type in C. reinhardtii to determine either spermatogenesis or oogenesis in V. carteri. Our findings establish genetic and evolutionary continuity between the mating-type specification and sex determination pathways of unicellular and multicellular volvocine algae, and will enable a greater understanding of how a transcriptional regulator, MID, acquired control over a complex developmental pathway.
Highlights
In many unicellular and simple multicellular eukaryotes sexual interactions are governed by mating types
In this study we investigated sex determination in the multicellular green alga Volvox carteri, a species with genetic sex determination; we established the relationship of V. carteri sexes to the mating types of its unicellular relative, Chlamydomonas reinhardtii
Theoretical work has suggested that sexual dimorphism could be acquired by linkage of gamete size-regulatory genes to an ancestral mating-type locus
Summary
In many unicellular and simple multicellular eukaryotes sexual interactions are governed by mating types. Among sexually reproducing organisms mating types are thought to have evolved before gamete size differences and separate sexes evolved [1,2]. The groundbreaking theory proposed by Parker and colleagues [7] modeled the evolution of anisogamy (asymmetric-sized gametes) from a starting population of isogametes (i.e., mating types) and identified the evolutionary forces that might cause a mating-type system to evolve into anisogamy (large and small gamete types) or oogamy (eggs and sperm). The genetic basis for the evolution of anisogamy/ oogamy has not been determined in any experimental system, and it is not known whether it requires the addition of size control genes or other genes to an ancestral mating locus as the model proposes
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