In group-living animals, grouping of conspecifics decreases mortality rate [28] and promotes nymphal development [28,29,30,31], egg production [32], and development of the related endocrine system [32, 33]. These phenomena have been referred to as the “group effect” or “effect of population density”.

Our study showed that a group effect is exerted not only on the reproductive mode of females, but also on the parthenogenetic mode of females. In the presence of sufficient resources, the group-housed females after the imaginal molt tended to produce parthenogenetic oothecae earlier and at more similar timings than did isolated females. Since shortening and synchronization of ootheca production cycle occurred not only in those housed in the same container, but also in those kept in different containers, the overall effect of promotion of ootheca production appears to reach a plateau for each individual, resulting in apparent synchronization of ootheca production. This assumption is supported by the finding that the shortening of the ootheca production cycle when five females were grouped was similar to that when three females were grouped. The cycle of parthenogenetic ootheca production is the fastest ever known in this species [19, 20, 33].

Ootheca production was significantly promoted when females were housed with virgin females but not when they were housed with genitalia-ablated males, suggesting that discrimination of cohabitants’ sex is a prerequisite for females to promote ootheca production. Ablation of the largest chemosensory organs, antennae, resulted in a delay in ootheca production compared to that in intact females, although complete ablation of the antennae may have side-effects related to loss of sensory input [34]. Unexpectedly, a typical female-specific odor, the primary sex pheromone component (periplanone-B), did not promote ootheca production, despite the fact that the female P. americana is equipped with a specific olfactory glomerulus in its first-order olfactory center that processes periplanone-B [35, 36].

Given that chemosensory signals are utilized for fine discrimination of the cohabitant status in cockroaches [21, 27], we suspect that sensing female-specific odors other than sex pheromones and/or sensing nonvolatile chemicals (e.g., hydrocarbons) [37] via antennal contact with females is most potent for promoting ootheca production. However, our data do not negate the possibility that mechanosensation is involved in the group effect. Although the values were below the significance threshold, some degree of shortening and synchronization of oothecae production occurred in females even without chemosensory organs. Given that tactile stimulation promotes ovary maturation in B. germanica [34, 38], tactile inputs from mechanosensory bristles distributed throughout the body and legs may complementarily promote asexual ootheca production.

On the level of endocrine control, juvenile hormone (JH) III released by the corpus allatum has a pivotal role in promoting the rate of vitellogenic growth and subsequent ootheca production in females [39]. In B. germanica, isolated virgin females have significantly lower rates of JH III synthesis than those in grouped females [40]. Further study is needed to evaluate whether JH III synthesis in P. americana is promoted more in group-housed females than in isolated females.

What is the functional significance of promotion of asexual ootheca production between females? Shortening of the ootheca production cycle contributes to an increase in parthenogenetic offspring produced by one female. Moreover, synchronizing egg production in grouped females may result in similar hatching timing of their offspring. Nymphs hatched synchronously would increase their fitness by aggregation and by sharing of resources, which could counter the lower hatching rate of parthenogenetic eggs than that of sexually produced eggs [19, 20].

In pre-social, domiciliary cockroaches, females of the same kin tend to aggregate in the same colony, whereas males leave the colony to avoid inbreeding [41]. Our behavioral observations are consistent with this finding; unmated females housed in the same container huddle close together with almost no fighting, whereas paired unmated males often fight until the antennae of both individuals are amputated (Nishino, personal observation). Thus, recognition of other virgin females and subsequent promotion of ootheca production might be the early stage of social cooperation that drives more prevalent parthenogenesis. This cooperative behavior is possibly succeeded by eusocial termites, five Reticulitermes species that found the first colony by female-female cooperation [13, 42].

As exemplified by P. surinamensis and P. subaptera, obligatory parthenogenesis very likely arises from facultative parthenogenesis in areas with low population densities. Females are advantageous over males for survival with low population densities. For example, females of P. americana, especially unmated ones, live longer than males [19, 43]. Due to their larger body masses, females are resistant to environmental changes, such as desiccation [9]. Thus, these traits of females appear to be suitable for adapting to new habitats with unfavorable conditions and maintaining female populations via parthenogenesis.

Maintaining certain populations of Periplaneta for more than four generations over a period of three years only by parthenogenesis is a threat to public health because of their potential roles as vectors for pathogens [44, 45] and allergens [46] indoors.

The fitness of parthenogens of P. americana is estimated to be higher than that of another species that uses facultative parthenogenesis, N. cineria, in which the clutch size of asexually produced offspring (3.2 ± 2.4) is much lower than that of sexually produced offspring (23.6 ± 4.2) and parthenogized progeny do not survive beyond the third generation [8]. Therefore, care should be taken for the possibility that a female-only colony of P. americana may be maintained locally, since benign but spatially isolated conditions can be created in sewage systems in most urban cities. Further investigation is clearly needed to determine whether the sustainability of a female-only colony is due to the inherent nature of wild individuals or to the genetic shift through artificial selection in our laboratory colonies.

One important but yet unsolved issue is whether the automictic parthenogenesis (meiosis and subsequent restoration by the doubling of chromosomes) opted by termites [13] is the case for more basal Blattoidea, P. americana. Microsatellite genotyping is needed to understand what kind of reproductive mode contributes to the maintenance of genotypic variance to counter the lower fitness of thelytoky parthenogenesis, and this is probably the key for a deeper understanding of why the genus Periplaneta is so abundant worldwide.