Going Solo: Discovery of the First Parthenogenetic Gordiid (Nematomorpha: Gordiida)

Abstract

Despite the severe fitness costs associated with sexual reproduction, its persistence and pervasiveness among multicellular organisms testifies to its intrinsic, short-term advantages. However, the reproductive assurance hypothesis predicts selection favoring asexual reproduction in sparse populations and when mate finding is difficult. Difficulties in finding mates is especially common in parasites, whose life cycles involve multiple hosts, or being released from the host into the external environment where the parasite can find itself trapped without a sexual partner. To solve this problem and guarantee reproduction, parasites in numerous phyla have evolved reproductive strategies, as predicted by the reproductive assurance hypothesis, such as hermaphroditism or parthenogenesis. However, this type of strategy has not been reported from species in the phylum Nematomorpha, whose populations have often been described as sparse. A new Nematomorpha species, Paragordius obamai n. sp., was discovered from Kenya, Africa, and appears to have solved the problem of being trapped without a mate by eliminating the need for males. Paragordius obamai n. sp. represents the first and only known species within this phylum to reproduce asexually. To determine the mechanism of this mating strategy, we ruled out the involvement of reproduction manipulating endosymbionts by use of next generation sequencing data, thus suggesting that parthenogenesis is determined genetically and may have evolved as a means to assure reproduction. Since this new parthenogenetic species and a closely related gonochoristic North American congener, P. varius, are easy to propagate in the laboratory, these gordiids can be used as model systems to test hypotheses on the genetic advantages and disadvantages of asexual reproduction and the genetic determinants of reproductive strategies in parasites.

Novel techniques for biodiversity studies of gordiids and description of a new species of Chordodes (Gordiida, Nematomorpha) from Kenya, Africa

“…Cysts were identified to genus based on size, folding pattern, and the presence or absence of visible spines. Based on morphology, most of these cysts were identified as belonging to the genus Paragordius (see Hanelt et al 2012) but we observed a few that morphologically resembled cyst descriptions of Chordodes morgani Montgomery 1898 and Chordodes janovyi Bolek, Schmidt-Rhaesa, Hanelt, & Richardson 2010(see Hanelt & Janovy 2002Bolek et al 2010). To isolate gordiid cysts from snails for cricket infections, the soft tissue was macerated with a razor blade.…”

“…at Oklahoma State University but died 71 or 72 DPE before worms emerged. These crickets contained double infections of the recently described P. obamai (see Hanelt et al 2012) and C. kenyaensis n. sp. All individuals of C. kenyaensis n. sp.…”

“…Over a one year sampling period no adult worms were found at any streams but cysts of three different types were recovered from aquatic snails from 32 of those streams. Additional studies by our group (Hanelt & Janovy 2002;Bolek & Coggins 2002;Bolek et al 2010;Hanelt et al 2012;Szmygiel 2012) on cyst morphology of six North American and African species of gordiids from three genera indicate that gordiid cysts can be useful in generic separation. Based on these observations, Hanelt et al (2012) collected Biomphalaria pfeifferi (Krauss 1848) snails infected with cysts of an unidentified species of Paragordius Camerano 1897 from Kenya, a country for which no gordiid records existed.…”

“…Additional studies by our group (Hanelt & Janovy 2002;Bolek & Coggins 2002;Bolek et al 2010;Hanelt et al 2012;Szmygiel 2012) on cyst morphology of six North American and African species of gordiids from three genera indicate that gordiid cysts can be useful in generic separation. Based on these observations, Hanelt et al (2012) collected Biomphalaria pfeifferi (Krauss 1848) snails infected with cysts of an unidentified species of Paragordius Camerano 1897 from Kenya, a country for which no gordiid records existed. After identification of the cyst to genus, and exposing the appropriate group of laboratory-reared arthropods, the first parthenogenetic species of gordiid, Paragordius obamai Hanelt, Bolek and Schmidt-Rhaesa 2012, was discovered.…”

“…Females of both the African C. janovyi and the North American C. morgani deposit egg strings in the water on twigs and detritus in a zigzag pattern, whereas females of the Asian Chordodes formosanus Chiu 2011 deposit their egg strings on rocks in a similar zigzag pattern. In contrast, the attachment of eggs strings to substrate has never been reported for other gordiid genera such as Gordius and Paragordius, which simply release egg strings into water (Hanelt & Janovy 2002;Hanelt et al 2012). Larvae and cysts of C. kenyaensis are also similar in morphology to other Chordodes species (C. formosanus, C. janovyi, C. morgani, and Chordodes japonensis Inoue 1952), but differ morphologically from larval and cyst stages of species of Paragordius and Gordius (see Schmidt-Rhaesa 1997;Bohall et al 1997;Bolek & Coggins 2002;Hanelt & Janovy 2002;Marchiori, et al 2009;Bolek et al 2010;Chiu et al 2011;Hanelt et al 2012).…”