Novel microsatellite markers suggest the mechanism of parthenogenesis in Extatosoma tiaratum is automixis with terminal fusion

Abstract

Parthenogenetic reproduction is taxonomically widespread and occurs through various cytological mechanisms, which have different impact on the genetic variation of the offspring. Extatosoma tiaratum is a facultatively parthenogenetic Australian insect (Phasmatodea), in which females oviposit continuously throughout their adult lifespan irrespective of mating. Fertilized eggs produce sons and daughters through sexual reproduction and unfertilized eggs produce female offspring via parthenogenesis. Here, we developed novel microsatellite markers for E. tiaratum and characterized them by genotyping individuals from a natural population. We then used the microsatellite markers to infer the cytological mechanism of parthenogenesis in this species. We found evidence suggesting parthenogenesis in E. tiaratum occurs through automixis with terminal fusion, resulting in substantial loss of microsatellite heterozygosity in the offspring. Loss of microsatellite heterozygosity may be associated with loss of heterozygosity in fitness related loci. The mechanism of parthenogenetic reproduction can therefore affect fitness outcomes and needs to be considered when comparing costs and benefits of sex versus parthenogenesis.

Sexually but not parthenogenetically produced females benefit from mating in a stick insect

“…Our finding that adult females of parthenogenetic origin were smaller than their sexually produced counterparts and exhibited signs of developmental instability in their wings is consistent with costs of high homozygosity. The extremely low heterozygosity generated by terminal fusion automixis in E. tiaratum (Alavi et al, 2018), and the consequent expression of recessive load could be responsible for the morphological patterns we observed, as has been suggested for similar developmental aberrations in other automictic taxa (Andersen et al, 2006; Schuett et al, 1997). Deviations from the normal phenotype due to reduced heterozygosity (as a result of inbreeding, automixis or other processes) could signify a general breakdown in developmental buffering (Lerner, 1954; Palmer & Strobeck, 1986; Vøllestad et al, 1999) and could negatively affect fitness‐related traits (Leary et al, 1985).…”

Development of microsatellite markers for the geographically parthenogenetic stick insect <i>Phraortes elongatus</i> (Insecta: Phasmatodea)

“…The complete loss of heterozygosity in the Shokawa population suggests that P. elongatus parthenogenesis is accomplished by automixis with terminal fusion, or gamete duplication. This is because offspring produced by parthenogenesis with terminal fusion or gamete duplication exhibit the loss of microsatellite heterozygosity, while parthenogens produced by automixis through central fusion or apomixis can maintain the same degree of heterozygosity as their mothers (Schwander and Crespi, 2009;Matsuura, 2017;Alavi et al, 2018). To date, in the facultatively parthenogenetic species of the stick insect order Phasmatodea, terminal fusion and gamete duplication have been reported in Extatosoma tiaratum (Macleay) (Alavi et al, 2018) and Bacillus rossius (Rossi) (Pijnacker, 1969), respectively.…”

“…This is because offspring produced by parthenogenesis with terminal fusion or gamete duplication exhibit the loss of microsatellite heterozygosity, while parthenogens produced by automixis through central fusion or apomixis can maintain the same degree of heterozygosity as their mothers (Schwander and Crespi, 2009;Matsuura, 2017;Alavi et al, 2018). To date, in the facultatively parthenogenetic species of the stick insect order Phasmatodea, terminal fusion and gamete duplication have been reported in Extatosoma tiaratum (Macleay) (Alavi et al, 2018) and Bacillus rossius (Rossi) (Pijnacker, 1969), respectively. Determination of P. elongatus parthenogenesis mechanisms will require cytological observations or detailed mother-offspring microsatellite analysis focusing on recombination, wherein the markers presented in the current study will be an essential tool.…”

Skipping sex: A nonrecombinant genomic assemblage of complementary reproductive modules

“…in angiosperms). [37,38,41,42,114] In all groups, genomic imprinting mechanisms like molecular modifications of centromere proteins (H3 and H4) can induce paternal chromosomal elimination. [115,116] In insects, the elimination of a sex chromosome or the full set of paternal chromosomes is linked to the formation of haploid males in cyclic parthenogens (e.g., scale insects, mites; [42] ).…”