The unusual reproductive system of head and body lice (Pediculus humanus)

Abstract

Insect reproduction is extremely variable, but the implications of alternative genetic systems are often overlooked in studies on the evolution of insecticide resistance. Both ecotypes of Pediculus humanus (Phthiraptera: Pediculidae), the human head and body lice, are human ectoparasites, the control of which is challenged by the recent spread of resistance alleles. The present study conclusively establishes for the first time that both head and body lice reproduce through paternal genome elimination (PGE), an unusual genetic system in which males transmit only their maternally derived chromosomes. Here, we investigate inheritance patterns of parental genomes using a genotyping approach across families of both ecotypes and show that heterozygous males exclusively or preferentially pass on one allele only, whereas females transmit both in a Mendelian fashion. We do however observe occasional transmission of paternal chromosomes through males, representing the first known case of PGE in which whole‐genome meiotic drive is incomplete. Finally, we discuss the potential implications of this finding for the evolution of resistance and invite the development of new theoretical models of how this knowledge might contribute to increasing the success of pediculicide‐based management schemes.

Nuclear Orthologs Derived from Whole Genome Sequencing Indicate Cryptic Diversity in the Bemisia tabaci (Insecta: Aleyrodidae) Complex of Whiteflies

“…The extensive observed inter-clade COI divergence was proposed to reflect an ancient evolutionary age, hypothesized to be about 86 million years ago (MYA) [26]. However, within insects, several haplodiploid groups or those with paternal genome elimination [94][95][96][97][98] have been shown to have substantially higher mitochondrial DNA substitution rates. For instance, in thrips [99], scale insects [100], book lice [101], and parasitic lice [102], divergences among congeneric species range from 10-25%.…”

Genetics and Genomics of an Unusual Selfish Sex Ratio Distortion in an Insect

“…So how did distortion evolve in Liposcelis? In booklice and their relatives, including parasitic lice, the baseline mode of sex determination is paternal genome elimination (PGE) [4,19], which has evolved independently in a number of terrestrial microarthropods [20]. Booklice that will develop into males fail to transmit any chromosomes that they inherit from their father.…”

Sexual antagonism in haplodiploids

“…Thus, we can see that, relative to eumendelian diploidy, haplodiploidy promotes the invasion of female beneficial alleles (and inhibits the invasion of male beneficial ones). In some haplodiploid species including mealybugs and body lice, imperfect PGE has been documented, such that in these species males do occasionally transmit paternalorigin genes (de la Filia et al 2018(de la Filia et al , 2019. As the amount of male paternal transmission increases, then males obtain an increasing share of the ancestry of future generations, and thus the relative importance of selection on males increases.…”

“…In natural populations levels of paternal escape are relatively low (in Planococcocus citri the proportion of paternal-transmission was estimated to be between 0.37-3.39%; de la Filia et al 2019), and thus invasion conditions are essentially identical to strict maternal transmission in males. Nonetheless, slight differences in the degree of leakage between populations, such as the differences documented between ecotypes of Pediculus humanus (de la Filia et al 2018), or potentially experimentally induced paternal-leakage, may allow for effective comparative tests.…”