A ZZ/ZW Sex Chromosome System in Cephalochordate Amphioxus

Abstract

Sex determination is remarkably variable among animals with examples of environmental sex determination, male heterogametic (XX/XY) and female heterogametic (ZZ/ZW) chromosomal sex determination, and other genetic mechanisms. The cephalochordate amphioxus occupies a key phylogenetic position as a basal chordate and outgroup to vertebrates, but its sex determination mechanism is unknown. During the course of generating Nodal mutants with transcription activator-like effector nucleases (TALENs) in amphioxus Branchiostoma floridae, serendipitously, we generated three mutant strains that reveal the sex determination mechanism of this animal. In one mutant strain, all heterozygous mutant offspring over three generations were female and all wild-type descendants were male. This pattern suggests the Nodal allele targeted is on a female-specific W chromosome. A second mutant showed the same W-linked inheritance pattern, with a female heterozygote passing the mutation only to daughters. In a third mutant strain, both male and female offspring could be heterozygous, but a female heterozygote passed the mutation only to sons. This pattern is consistent with the targeted allele being on a Z chromosome. We found an indel polymorphism linked to a Nodal allele present in most females, but no males in our cultured population. Together, these results indicate that Nodal is sex chromosome-linked in B. floridae, and that B. floridae has a ZZ/ZW sex chromosome system.

Three amphioxus reference genomes reveal gene and chromosome evolution of chordates

“…S37 ), but do not exhibit sexually differentiated patterns of mapped read coverage. These results together indicated that all three amphioxus species have independently evolved female heterogametic sex chromosomes, and the result of Bf is consistent with a recent genetic study ( 59 ).…”

Diversity of Modes of Reproduction and Sex Determination Systems in Invertebrates, and the Putative Contribution of Genetic Conflict

“…In other groups, such as Lepidoptera or parasitic flatworms from the genus Schistosoma, sex is determined by a ZW system, with ZZ individuals being males and ZW (or Z0) individuals being females. Such a system was also recently reported in the lancelet Branchiostoma floridae [63]. Depending on the clade, sex chromosomes can be highly conserved, as in Lepidoptera where the ZW pair has been conserved for more than 230 Myr [64], or can vary greatly even between sister families, as in Diptera where new sex chromosomes have appeared at least seven times in less than 300 Myr [65].…”

Three amphioxus reference genomes reveal gene and chromosome evolution of chordates

“…The sex-determination (SD) mechanisms of amphioxus remain largely enigmatic, with no cytogenetic evidence for the existence of differentiated sex chromosome pair in Bf and Bb ( 19, 47 ). A recent genetic study suggested that Bf has a female heterogametic sex chromosome system (male ZZ, female ZW) ( 48 ). We confirmed this by generating a heterozygous female mutant strain of Pitx with transcription activator-like effector nucleases (TALENs), whose mutant alleles are only carried by their daughters.…”