oskar Predates the Evolution of Germ Plasm in Insects

Abstract

oskar is the only gene in the animal kingdom necessary and sufficient for specifying functional germ cells. However, oskar has only been identified in holometabolous ("higher") insects that specify their germline using specialized cytoplasm called germ plasm. Here we show that oskar evolved before the divergence of higher insects and provide evidence that its germline role is a recent evolutionary innovation. We identify an oskar ortholog in a basally branching insect, the cricket Gryllus bimaculatus. In contrast to Drosophila oskar, Gb-oskar is not required for germ cell formation or axial patterning. Instead, Gb-oskar is expressed in neuroblasts of the brain and CNS and is required for neural development. Taken together with reports of a neural role for Drosophila oskar, our data demonstrate that oskar arose nearly 50 million years earlier in insect evolution than previously thought, where it may have played an ancestral neural role, and was co-opted to its well-known essential germline role in holometabolous insects.

Genome of Rhodnius prolixus , an insect vector of Chagas disease, reveals unique adaptations to hematophagy and parasite infection

“…Of note, the germ plasm genes osk and valois (vls) were absent from R. prolixus. The absence of osk likely reflects a gene loss in insect evolution, because it was present in the transcriptome of the basally branching cricket Gryllus bimaculatus (27), where it was incorporated during neural development. Among the embryonic AP genes, Kruppel (RPRC000102) and giant (RPRC001027) were functionally confirmed as gap genes (28,29).…”

The Crystal Structure of the Drosophila Germline Inducer Oskar Identifies Two Domains with Distinct Vasa Helicase- and RNA-Binding Activities

“…Residues involved in dimerization (green inverted triangle) of the Drosophila Oskar (legend continued on next page) upon which the germ plasm is assembled, by stepwise recruitment of other components. Although the oskar gene is only present in some insects, germ plasm has been described in many species (Juhn and James, 2006;Juhn et al, 2008;Lynch et al, 2011, Ewen-Campen et al, 2012Voronina et al, 2011;Schisa, 2012). In Danio rerio, Bucky ball, and in C. elegans, PGL-1 and PGL-3 have been shown to have central roles in germ plasm formation (Marlow and Mullins, 2008;Bontems et al, 2009;Updike and Strome, 2010).…”

The evolution of insect germline specification strategies

“…Thus, it was a major surprise when an osk ortholog was discovered in the hemimetabolous cricket Gryllus, proving that this gene has a much longer evolutionary history than previously appreciated [12]. This discovery was particularly unexpected because Gryllus lacks any evidence of maternal germ plasm [13,14].…”