Evidence for Sex and Recombination in the Choanoflagellate Salpingoeca rosetta

Abstract

Summary Nearly all animals reproduce sexually through the production and fusion of sperm and egg cells, yet little is known about the ancestry of animal sexual reproduction. Moreover, the sexual cycle of the closest living relatives of animals, the choanoflagellates [1, 2], remains completely unknown. The choanoflagellate Monosiga brevicollis, possesses a “meiotic toolkit” of genes [3], but the lack of polymorphisms detected during genome sequencing precluded inferences about its ploidy or sexual cycle [1]. Here we report that a related choanoflagellate, Salpingoeca rosetta [4, 5], has a sexual life cycle and transitions between haploid and diploid states. Haploid cultures of S. rosetta became diploid in response to nutrient limitation. This ploidy shift coincided with anisogamous mating, during which small, flagellated cells fused with larger flagellated cells. Distributions of polymorphisms in laboratory strains of S. rosetta provided independent evidence of historical recombination and mating. The ability of S. rosetta to produce morphologically differentiated gametes and to engage in sexual reproduction has implications both for reconstructing the evolution of sex in the progenitors of animals and for establishing classical genetics in choanoflagellates.

Circumstantial evidence of life history events in loricate choanoflagellates

“…The life history of Salpingoeca rosetta thus comprises at least five different cell types (Dayel et al, 2011;Levin and King, 2013).…”

“…Levin and King (2013) recently demonstrated that Salpingoeca rosetta can switch ploidy under laboratory conditions as part of a sexual life cycle that involved several morphotypes.…”

The origin and evolution of synaptic proteins – choanoflagellates lead the way

“…plasmids, proteins) into choanoflagellate cells, as many choanoflagellate species are covered by a thick extracellular matrix (Dayel et al, 2011). However, key advances have recently been made in establishing classical genetics in choanoflagellates, as the choanoflagellate S. rosetta produces morphologically differentiated gametes and engages in sexual reproduction (Levin and King, 2013;Levin et al, 2014). These studies together with the findings described here provide the first evidence that choanoflagellates may serve as a simple model for discovering ancestral functions of synaptic proteins.…”

Bacterial Influences on Animal Origins

“…A modern example of transient cell differentiation can be found in the choanoflagellate S. rosetta, which produces diverse unicellular and colonial morphotypes in response to a variety of environmental cues (Fig. 4C) (Dayel et al 2011;Alegado et al 2012;Levin and King 2013). One of the colonial morphotypes, the rosette colony, has been shown to undergo development involving multiple layers of regulation.…”