At its simplest, life history theory postulates that organismal fitness is the consequence of a series of physiological and behavioral trade-offs that result in a negative correlation among individual life history traits. This is the consequence of devoting resources toward one process, such as growth or reproduction, at the expense of other processes, such as maintenance (Stearns 1989, Zera and Harshman 2001). Indeed, life history trade-offs have been well documented within multiple species of both vertebrates (Jimenez 2016, Jimenez et al. 2014) and invertebrates (Haag 2013, Ramirez Llodra 2002). They typically involve reduced growth, developmental delays, and/or reduced survival in conjunction with a reciprocal increase in reproductive success and vice versa. Insects have been especially useful for studying the genetic and biochemical bases for these trade-offs with Drosophila melanogaster Meigen and the cricket, Gryllus firmus Scudder, serving as the dominant models (Bai et al. 2015, Harshman et al. 1999, Rose 1984, Rose and Bradley 1998, Zera and Larsen 2001, Zera and Zhaol 2003). Similar outcomes have been reported in other species, such as grasshoppers (Hatle et al. 2013), beetles (Trumbo and Robinson 2004, Boman et al. 2008), and cockroaches (Barrett et al. 2009, Jensen et al. 2016, Moore and Sharma 2005). In general, there is a marked relationship between adult body mass and a suite of life history traits within multiple species (Shingleton 2011).

Within insects, body size is an excellent predictor of reproductive capacity (Honek 1993), although environmental factors can impose a high degree of intraspecific variation (Davidowitz 2008). Large females are markedly more fecund than smaller counterparts (Davidowitz 2008, Honek 1993, Jimenez-Perez and Wang 2004, Maxwell and Frinchaboy 2014), while large males enjoy improved mating success. This is the result of increased attractiveness to females and/or increased success during male–male competition (reviewed in Hunt et al. 2009). In addition, within cinereous cockroaches there is a negative correlation between male adult body mass and female gestational period. This effectively increases the number of offspring produced by larger males (Schimpf et al. 2012). As a whole, this suggests there is a selective advantage for large size among individuals of both sexes within cinereous cockroaches and, perhaps, insects in general.

When the legs of an insect lose contact with a substrate, a reflexive righting program (i.e., the righting response) is initiated to restore dorsoventral orientation (Frantsevich 2004 and references therein). Within cockroaches, this response is characterized by dorsal flexion in conjunction with rhythmic bursting of the motor neurons controlling leg movement resulting in a “flailing” motion that allows individual legs to contact the substrate (Camhi 1977, Zill 1986). In an ideal scenario, the forces generated by those legs in contact with the substrate may then be sufficient to cause righting of the animal (Full et al. 1995). Importantly, the righting response is conserved among terrestrial and semiterrestrial species given the myriad situations that could result in an individual being overturned. For example, individuals may fall from an elevated substrate or be turned over due to an aggressive encounter with a conspecific thereby rendering them vulnerable to predation, or simply leaving them stranded and subject to environmental stressors (Golubovic et al. 2013, Penn and Brockman 1995). Indeed, the ability to initiate and complete the righting response has often been cited as an indicator of organismal fitness, but with some caveats (Davy et al. 2014).

Here, we examined the effect of body size on the speed of the righting response within male and female cinereous cockroaches, Nauphoeta cinerea (Olivier), with differing reproductive histories. In this study, individuals collected from mass colonies were presumed mated, while individuals maintained as singly housed adults from the day of adult emergence were considered virgins. Despite the fact that some females within this species have the capacity for facultative parthenogenesis (Corley et al. 2001, Moore and Moore 2003), nymphs were never observed in the containers housing individual females used for this study.

Materials and Methods

Results

Female cinereous cockroaches were significantly heavier than their male counterparts, regardless of the colony condition (two-sample t test, P < 0.04 for all). They also tended to be longer, although this difference was not always significant. Finally, we found that the body size index of the females was always significantly greater than that of the males (two-sample t test, P ≤ 0.01) with the exception of those individuals from Cohort 2 (Table 1).

Table 1 Body length, body mass and body size index (mean ± SEM) for male and female cinereous cockroaches of either mixed (mass colony) or known age (cohorts). P values indicate statistical significance after two-sample t test.

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Two-way analysis of variance indicated a significant effect of both age (cohort) and sex on righting time in the known-age individuals. In particular, there was a significant main effect of age for each of the three morphological measures (body mass, body length, and body size index; P < 0.01 for all); older individuals were significantly larger. There was also a significant main effect of sex for body mass and body size index only (P < 0.001) in that female cockroaches were larger than males. The main effect of sex on body length was not statistically significant (P = 0.058). The cohort × sex interaction term was also not significant for any comparison (P > 0.6) (Table 2).

Table 2 Effect of age (cohort) and sex on body mass, body length, and body size index in virgin cinereous cockroaches. A full-factorial two-way analysis of variance was constructed separately for each measure.

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Interestingly, the reproductive history of individual cockroaches modulated this response in a sex-specific manner. In particular, the righting time of female cockroaches from the mass colonies was slower than that of similarly housed males, while the opposite was true for singly housed individuals of known age. In other words, the righting times of females from the mass colonies were slower than that of males raised under identical conditions per unit of measure. On the other hand, singly housed males had a slower righting time than singly housed females per unit of measure (Fig. 1). Unfortunately, the relatively small sample sizes (n = 12 to 27) precluded performing these analyses within the individual cohorts.

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In the group-housed insects, an analysis of covariance (ANCOVA) indicated that the effect of body length, body mass, and body size index was significant for each measure (P < 0.001), as well as the effect of sex (P < 0.001). Meanwhile, in singly housed individuals, ANCOVA indicated a significant effect of only body mass, body size index, and sex on individual righting times (P ≤ 0.01 for all); body length had no effect on righting time. Although the specific reproductive history of individuals sampled from the mass colony was unknown, they were presumed to have mated while the singly housed individuals were never in the presence of the opposite sex posteclosion. Since individuals of this species are not reproductively mature until at least 6 d old (Corley et al. 2001, Moore and Moore 2003), it is reasonable to assume that singly housed cockroaches were virgins at the time of testing.

Lastly, it appeared there was a significant effect of age (cohort) at the time of testing on the righting time within the singly housed individuals (data not shown). However, given that body length, body mass, and the body size index were greater as the age of the individuals increased regardless of sex (Table 1), we chose to reevaluate the effect of age on righting time after adjusting for the age-specific variation in each of these measures. In brief, the relationship between the residuals of the righting time (after adjustment for age) and each of the morphological measures (also after adjustment for age) was assessed using simple linear regression (as in Speakman 2005). For both males (P ≥ 0.35) and females (P ≥ 0.13), the apparent effect of age on righting time was not observed after this adjustment (not shown).

Discussion

Despite its use as an indicator of fitness in vertebrates (Davy et al. 2014), the righting response remains underutilized within invertebrates. Our data indicate that simple morphological measures are correlated with the ability of cinereous cockroaches to right themselves under controlled conditions, and that larger individuals were slower to right themselves (Fig. 1). This relationship may reflect a trade-off between body size and reproduction given that the reproductive success of larger individuals of both sexes is greater and, taken together, these data suggest that increased fecundity may come at a cost. In addition, we found the presumed reproductive history of the individuals further modulated this response or, more specifically, that virgin females were quicker to right themselves on a per-unit-of-measure basis relative to virgin males while the opposite was true for individuals that were presumed to be mated (Fig. 1).

In general, we found that individual body mass, as well as the individual body size indices, were the best predictors of the righting time in each sex regardless of the insect condition. Presumably, this reflects the need to generate more force at the time the leg contacts the substrate for larger individuals to right themselves. Moreover, given the righting response in cockroaches relies on a standardized, yet somewhat uncoordinated, flailing of the legs, the longer time to righting may be a consequence of chance (Full et al. 1995). That is, it may simply require more time for the legs to contact the substrate “just right” in order to generate the force needed for larger individuals to right themselves (Faisal and Matheson 2001). Meanwhile, the lack of a relationship between body length and the righting time of individual cockroaches is likely the consequence of their body plan. In particular, cockroaches have broad, flattened bodies in conjunction with relatively short legs; hence, the total length of the individual is unlikely to influence the likelihood of the tarsi contacting the substrate (Faisal and Matheson 2001). Since we did not collect any measures of either body (e.g., pronotum) width or leg (e.g., femur) length, we are unable to determine whether these measures are important determinants of righting times within this species.

Overall, the relationship between morphological measures and the righting response has gone largely unexplored in both vertebrates and invertebrates. Instead, the emphasis has centered largely on deducing the developmental effects of various environmental factors, and their subsequent impact on measures of locomotor ability, including righting times. Not surprisingly, developmental derangements often have an adverse effect on the righting response within multiple species (Farkas et al. 2009, Hurst et al. 2014, Sim et al. 2015).

As with any organism exhibiting determinant growth, the final body size of cockroaches at adulthood is a fixed trait, and this is especially true for linear measures such as body length. Hence, we believe the apparent age-related increase in both body mass and body length in our singly raised adult population is an artifact of changes in housing conditions with time (Table 2). In particular, known-age individuals used in this study were collected directly from the mass colonies at approximately 5–6-mo intervals; however, these colonies were maintained in the absence of active population control. Consequently, the density within each colony notably increased with time, thereby reducing resource availability to the developing immatures in the younger cohorts. The detrimental effect of resource limitation on growth rates and final body size is well known (Abrams et al. 1996, Dmitriew 2011). Importantly, after accounting for the age (cohort)-specific variation (Table 1), we found no effect of aging on righting times in cinereous cockroaches. This lack of an effect on righting times is consistent with a previous study examining aging and locomotor behavior in other species of cockroaches (Ridgel et al. 2003).

Given that larger individuals of both sexes were slower to right themselves, and that larger individuals within insects typically enjoy increased reproductive success, these data suggest that body size variation may represent a life history trade-off within cinereous cockroaches or, more specifically, that increased reproductive success associated with larger body sizes comes at a risk. In particular, there is an increased likelihood of mortality should a large individual become overturned relative to a smaller individual. Although the degree to which this happens in nature is unknown, we commonly see individual cockroaches on their backs within the group-housed laboratory populations (J.M.H. pers. obs.).

Furthermore, since female cinereous cockroaches are ovoviviparous, a substantial proportion of their adult body mass is attributable to the presence of mature ovarioles and/or ootheca within mated individuals. More interestingly, resource limitation within this species is actually associated with an increase, not a decrease, in female fecundity (Barrett et al. 2009). Consequently, the largest females from the mass colonies should enjoy the greatest reproductive success despite having the slowest righting response on per-unit measures of body mass, body length, or body size index. Meanwhile, the largest singly housed males should have the greatest potential for reproductive success if given the opportunity, even if they are slower to right themselves on a per-unit basis. Further support for this idea is provided by the occurrence of oosorption within unmated females of this species (Barrett et al. 2009). This would reduce the burden associated with reproductive organ size in unmated females.

Ultimately, these data were collected with the goal to determine whether aging had an effect on the righting response within this species, as well as whether the effect of age varied with sex. They were not collected to address hypotheses concerning differences in body size among individual cockroaches and their effects on the righting response. It was only during preliminary analyses that the specific relationship between morphological measures and righting times was observed, as well as the sex-dependent variation in the speed of the response. This led us to expand our initial dataset to include individuals from each of the reproductive conditions to corroborate, or refute, our initial findings. Unfortunately, this means meaningful data, for example additional morphometric measures or fecundity data from tested individuals, are lacking. Nonetheless, we believe they make a compelling argument for an unappreciated role of body size and reproductive history on life history trade-offs within cockroaches.

In conclusion, we found that body size, and especially body mass, has a significant effect on the righting ability of both sexes of the cinereous cockroach. Larger individuals, which are typically more fecund, are slower to right themselves. In addition, our data suggest that reproductive history further modulates this response in a sex-specific manner or, more specifically, that mated females are slower to right themselves relative to same-sized males while virgin females are quicker to right themselves relative to same-sized virgin males. Presumably, this is a reflection of the burdens imposed by the increased weight of the maturing ovarioles and/or the developing brood within the mated females of this ovoviviparous species.