Arrhenotoky and oedipal mating in the northern fowl mite (Ornithonyssus sylviarum) (Acari: Gamasida: Macronyssidae)

Abstract

BackgroundThe northern fowl mite (NFM; Ornithonyssus sylviarum) is a blood-feeding ectoparasite of birds and a major pest of poultry in the United States. Mite populations spread rapidly in commercial flocks, reach peak burdens of >70,000 mites per bird and have developed resistance to many pesticides. Despite decades as a pest in the United States, the reproductive biology of NFM remains unclear. Based on karyotypes, the NFM has haplodiploid sex determination, which suggests unmated females could produce male offspring (arrhenotoky). Thus, unmated females could disseminate to a new host and initiate an infestation by producing and mating with sons (oedipal mating).MethodsWe used small capsules to isolate and recover NFM on host chickens. Mites in capsules could blood feed, develop and reproduce, but could not contact other mites. Individual larvae were matured in isolation to produce known, unmated females. We evaluated reproduction of (I) previously mated females (i) in isolation, or (ii) paired with a male, and (II) unmated (virgin) females in isolation. In each treatment we recorded the number and sexes of offspring produced over time.ResultsMated NFM produced female and male offspring in isolation, or when paired with a male. When paired with a male, females produced a female-biased sex ratio of the offspring (F:M ratio ~5:1). Unmated, female NFM produced exclusively male offspring when in isolation. When paired with their sons that had developed to maturity, the "virgin" females were able to mate and subsequently produce female offspring.ConclusionsThis study found that females with immediate access to sperm produced mostly female offspring. Virgin female NFM initially produced only male offspring and subsequently used oedipal mating to produce female offspring. Using this reproductive system NFM could successfully colonize new hosts as immature, or unmated females. The strong female-biased sex ratio of NFM populations suggests a large proportion of the parasite population is capable of disseminating to new hosts, which is essential for an obligate parasite to persist.

Reproductive parameters of female Varroa destructor and the impact of mating in worker brood of Apis mellifera

“…Instead, reproduction by virgin females (parthenogenesis) is a common phenomenon (Oliver 1971;Kiszewski et al 2001). In certain cases, e.g., the northern fowl mite (McCulloch and Owen 2012), the two-spotted spider mite (Tuan et al 2016) or the rice tarsonemid mite (Xu et al 2001) virgin females are able to produce male offspring and even reproduce bisexual offspring after mother-son mating, so-called oedipal mating (McCulloch and Owen 2012). As sex determination in V. destructor is regulated via haplodiploidy, it was examined if unmated Varroa females might be able to produce haploid (male) offspring without prior mating as well ).…”

Comparative in vitro evaluation of contact activity of fluralaner, spinosad, phoxim, propoxur, permethrin and deltamethrin against the northern fowl mite, Ornithonyssus sylviarum

“…Two major ectoparasite species severely affect the poultry industry worldwide: the northern fowl mite, Ornithonyssus sylviarum , and the poultry red mite, Dermanyssus gallinae [ 1 , 2 ]. Both mite species are obligate hematophagous parasites able to complete their life-cycles within about 1 week under optimal conditions [ 2 – 4 ]. Mite populations can become dense very quickly in commercial poultry facilities reducing hen performance and profitability [ 5 , 6 ].…”

Demographic analysis of arrhenotokous parthenogenesis and bisexual reproduction of Frankliniella occidentalis (Pergande) (Thysanoptera: Thripidae)

“…Arrhenotoky with oedipal mating is not only important to dispersion, colonization and sex allocation 47 , but is also an important aspect in genetics and evolution 48 . It has previously been reported in mites 30 , 46 , parasitoid wasps 49 , and thrips 50 . Several important pest species, including F. occidentalis and the worldwide distributed two-spotted spider mite ( Tetranychus urticae Koch), are capable of reproducting in this manner.…”

“…Arrhenotokous reproduction is a unique biological process, all unfertilized eggs are haploid and develop as males, while fertilized eggs are diploid and develop as females. This process enables virgin females to survive and produce male offspring, which, in turn, build a bisexual cohort through oedipal mating (mating with their sons) 46 . Arrhenotoky with oedipal mating is not only important to dispersion, colonization and sex allocation 47 , but is also an important aspect in genetics and evolution 48 .…”