The NFM is a cosmopolitan ectoparasite of birds and an economic pest of the poultry industry in the United States[1, 2]. Populations of NFM are typically female-biased and past karyotyping suggested the NFM has haplodiploid sex determination[4, 7]. This study determined that male NFM are produced from unfertilized eggs (arrhenotoky) and that virgin females are able to produce and mate with sons (oedipal mating) to subsequently produce female offspring. These observations are relevant to the epidemiology of NFM outbreaks in commercial poultry flocks. For sexually reproducing parasites to establish on a new host the dispersing females must be mature and mated, or must colonize a new host with males[8, 10]. Transmission of NFMs between hosts begins early during an infestation when there are relatively few mites (low mating opportunity) and many individuals may be immature. Oedipal mating provides a way for female NFMs to disseminate to new hosts without being constrained by mating opportunity, or sexual maturity. This makes all females, regardless of stage, capable of establishing on a new host. For an obligate parasite this high transmission potential represents a tremendous ecological advantage.
Mated females in isolation were able to produce daughters for up to 14 days. Under natural conditions mated NFMs may produce daughters over a longer period. The ability of females to store sperm could also enhance the transmission potential of NFMs. Sperm storage reduces the necessity for males since females may not need repeated insemination throughout reproductive maturity. As a result, the population can persist with a strong female-biased sex ratio (i.e. a maximum number of transmissible individuals). Although NFMs reside on the host bird for the entire life cycle, they are able to survive off-host for up to 35 days. The ability to store sperm extends the capacity of dispersing NFMs to establish new infestations.
The reproductive biology of NFM is also informative to basic studies of arrhenotoky, mate competition and adaptation. Cruickshank and Thomas tested the hypothesis that arrhenotoky evolves from a pseudo-arrhenotokous ancestral state, using a phylogenetic study of Mesostigmatid mites. Our determination that NFM, a member of this group, is arrhenotokous supports their conclusion. Female biased sex ratios can be explained by conditions of local mate competition, where small, isolated populations founded by a few females produce selection for a female-biased sex ratio. This has empirical support from studies of the spider mite, which is also haplodiploid and arrhenotokous[22, 23]. Populations of NFM are produced by few founders and are aggregated on the host body. Thus, NFM may represent another system where the effects of local mate competition have shaped reproductive biology. Finally, haplodiploidy provides a hypothetical advantage for adaptation because deleterious alleles may be lost rapidly through males[24, 25]. The NFM has demonstrated a remarkable ability to adapt to different host species and pesticide pressure. Here too, the NFM may prove a useful taxon to explore the basic evolutionary implications of haplodiploidy.
In other haplodiploid mite systems (e.g. spider mites) it is possible for mated females to selectively adjust the sex ratio of offspring, depending on resource availability and mating opportunities[5, 23]. It is not clear from our study if NFM females actively manipulate sex ratio. Captured females paired with males produced more daughters than captured females in isolation. While this suggests that females in proximity to males may produce more daughters, experiments 2 and 3 indicate that NFMs do not manipulate offspring sex ratios. Previously mated females (experiment 2) isolated without a mate for an extended period of time produced strongly female-biased offspring. Pairing of virgin females with a son (experiment 3) resulted in few female offspring and a roughly balanced sex ratio. Macke et al. noted that sex ratio control of Tetranychus mites changed with female age and the number of mating events. The ages and frequency of mating were unknown for the NFMs we collected from intact infestations. The sex ratios of offspring in experiment 3 may have been affected by using mites that were too old or were perhaps influenced by prolonged reproduction without males. Additional experiments will be required to determine what factors impact female versus male production by mated NFMs. Another factor that could contribute to sex ratio control in the NFM is sex-distorting endosymbionts (e.g. Wolbachia)[26, 27]. The mites used in our study came from a colony closed to immigration for several hundred generations that did not test positive by PCR screening for the endosymbionts Wolbachia, Spiroplasma or Cardinium. Nonetheless, it is possible that endosymbiotic bacteria could play a role in the reproductive biology of field populations of this ectoparasitic mite.