Group-housed females promote production of asexual ootheca in American cockroaches

Abstract

BackgroundFacultative parthenogenesis, seen in many animal phyla, is a reproductive strategy in which females are able to generate offspring when mating partners are unavailable. In some subsocial and eusocial insects, parthenogenesis is often more prevalent than sexual reproduction. However, little is known about how social cooperation is linked to the promotion of parthenogenesis. The domiciliary cockroach Periplaneta americana is well-suited to addressing this issue as this species belongs to the superfamily Blattoidea, which diverged into eusocial termites and shows facultative parthenogenesis.ResultsWe studied environmental factors that influence asexual production of ootheca using behavioral assays in P. americana. When more than three virgin females immediately after the imaginal molt were kept together in a small sealed container, they tended to produce egg cases (oothecae) via parthenogenesis earlier than did isolated females, resulting in apparent synchronization of ootheca production, even among females housed in different containers. In contrast, virgin females housed with genitalia-ablated males or group-housed females with antennae ablated did not significantly promote ootheca production compared to isolated females. Daily addition of the primary sex pheromone component to the container did not promote ootheca production in isolated females. Another line of study showed that grouped females make parthenogenesis more sustainable than previously known; a founder colony of 15 virgin females was sufficient to produce female progeny for a period of more than three years.ConclusionsGroup-housed females promote and stabilize asexual ootheca production compared to isolated females, and that this promotion is triggered by female-specific chemosensory signals (other than sex pheromone) primarily detected by antennae. Promotion of ootheca production between females is likely to be an early stage of social cooperation, reminiscent of the foundation and maintenance of a colony by female pairs in the eusocial termite Reticulitermes speratus.Electronic supplementary materialThe online version of this article (doi:10.1186/s40851-017-0063-x) contains supplementary material, which is available to authorized users.

Distribution of Galepsus spp. in Southern Africa and Life History of Galepsus lenticularis (Mantodea: Tarachodidae)

“…However, the difference observed in G. lenticularis oothecae (unhatched and hatched and unfertilized) with regard to the number of eggs and length of the oothecae could indicate that these females would rather conserve valuable resources, instead of producing unfertilized oothecae which do not produce offspring. In contrast to this, a recent study [48] indicated that the length of the ootheca of a cockroach species (Periplaneta americana) Linnaeus 1758 (Blattodea: Blattidae), was not influenced by the fertility of the oothecae. Although P. americana can also reproduce through parthenogenesis, it is highly likely that females would not invest valuable resources into formation of oothecae if it produces no genetically diverse offspring.…”

First molecular genetic evidence for automictic parthenogenesis in cockroaches

“…We first investigated whether female adults of P. americana can reproduce parthenogenetically by individually rearing female nymphs from the laboratory colony. As previously reported (Takahashi, ; Roth & Willis, ; Xian, ; Katoh et al ., ), many of the virgin female adults (17 out of 23 adults, 73.9%) produced oothecae without mating.…”

“…Although the hatchability of parthenogenetic nymphs was low, we found that, once hatched, most of parthenogenetic nymphs grew well, without apparent abnormalities, regardless of the extremely low levels of genetic heterozygosity expected among them. Indeed, a recent study showed that the parthenogenetic offspring of P. americana are fertile and can produce offspring via thelytoky; a "female-only" parthenogenetic colony has been maintained in this manner for approximately 3 years (approximately six generations) (Katoh et al, 2017). This suggests that P. americana can potentially reproduce almost normally without sexual reproduction if recessive deleterious alleles are purged.…”

“…With very few exceptions, cockroaches do not produce offspring parthenogenetically in nature. However, under artificial conditions, for example, separation of females from males, thelytoky has been reported in several species, including Periplaneta americana (Takahashi, ; Roth & Willis, ; Xian, ; Katoh et al ., ), P. brunnea (Willis et al ., ), Blatta orientalis (Roth & Willis, ), Ectobius lapponicus (Brown, ), E. pallidus (Brown, ), Nauphoeta cinerea (Corley et al ., ; Corley et al ., ), and Pycnoscelus surinamensis (Roth, ). Conversely, attempts to obtain parthenogenetic offspring in the German cockroach Blattella germanica have been unsuccessful (Roth & Willis, ; Xian, ).…”

“…With very few exceptions, cockroaches do not produce offspring parthenogenetically in nature. However, under artificial conditions, for example, separation of females from males, thelytoky has been reported in several species, including Periplaneta americana (Takahashi, 1924;Roth & Willis, 1956;Xian, 1998;Katoh et al, 2017), P. brunnea (Willis et al, 1958), Blatta Correspondence: Takaaki Daimon, Department of Applied Biosciences, Graduate School of Agriculture, Kyoto University, Kitashirakawa Oiwakecho, Sakyo-ku, Kyoto 606-8502, Japan. Tel/fax: +81 75 753 6308; email: daimon.takaaki.7a@kyotou.ac.jp orientalis (Roth & Willis, 1956), Ectobius lapponicus (Brown, 1973), E. pallidus (Brown, 1973), Nauphoeta cinerea (Corley et al, 1999;Corley et al, 2001), and Pycnoscelus surinamensis (Roth, 1967).…”