Population biology of a selfish sex ratio distorting element in a booklouse (Psocodea: Liposcelis)

Abstract

Arthropods harbour a variety of selfish genetic elements that manipulate reproduction to be preferentially transmitted to future generations. A major ongoing question is to understand how these elements persist in nature. In this study, we examine the population dynamics of an unusual selfish sex ratio distorter in a recently discovered species of booklouse, Liposcelis sp. (Psocodea: Liposcelididae) to gain a better understanding of some of the factors that may affect the persistence of this element. Females that carry the selfish genetic element only ever produce daughters, although they are obligately sexual. These females also only transmit the maternal half of their genome. We performed a replicated population cage experiment, varying the initial frequency of females that harbour the selfish element, and following female frequencies for 20 months. The selfish genetic element persisted in all cages, often reaching very high (and thus severely female‐biased) frequencies. Surprisingly, we also found that females that carry the selfish genetic element had much lower fitness than their nondistorter counterparts, with lower lifetime fecundity, slower development and a shorter egg‐laying period. We suggest that differential fitness plays a role in the maintenance of the selfish genetic element in this species. We believe that the genetic system in this species, paternal genome elimination, which allows maternal control of offspring sex ratio, may also be important in the persistence of the selfish genetic element, highlighting the need to consider species with diverse ecologies and genetic systems when investigating the effects of sex ratio manipulators on host populations.

When does the female bias arise? Insights from the sex determination cascade of a flea beetle with a strongly skewed sex ratio

“…Strongly distorted sex ratios as observed here in A. lythri may be caused by genomic conflicts over sex chromosomes or sex-determining factors (Perlman et al 2015 ). Two types of selfish genetic elements are known to manipulate the sex of their hosts: cytoplasmic inherited endosymbionts (like Wolbachia , Rickettsia , Spiroplasma , and Cardinium ) and selfish genetic elements on sex chromosomes (Hodson and Perlman 2019 ). In addition, mitochondria as cytoplasmic elements may also benefit the female sex to the expense of males (Burt and Trivers 2006 ; Perlman et al 2015 ), as has been repeatedly shown for cytoplasmic male sterility in plants (He et al 2021 ; Wang et al 2022 ).…”

Asymmetric Inheritance: The Diversity and Evolution of Non-Mendelian Reproductive Strategies

“…2). Liposcelis booklice, a genus with PGE and parthenogenesis, also has some females with only maternal genome transmission, most likely a type of hybridogenesis (Hodson & Perlman 2019;Hodson et al 2017;Mockford 1971) In many cases, new patterns of asymmetric inheritance emerge within clades that are already asymmetric. Examples include the co-occurence of PGE and germline restricted chromosomes in the gall midges and fungus gnats, or the B chromosomes in mealybugs which exploit the transmission asymmetry of PGE to enhance their own transmission.…”