Research Article |
Corresponding author: Kevin A. Judge ( judgek3@macewan.ca ) Academic editor: Juliana Chamorro-Rengifo
© 2017 Janice J. Ting, Kevin A. Judge, Darryl T. Gwynne.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Ting JJ, Judge KA, Gwynne DT (2017) Listening to male song induces female field crickets to differentially allocate reproductive resources. Journal of Orthoptera Research 26(2): 205-210. https://doi.org/10.3897/jor.26.19891
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Differential investment in offspring by mothers is predicted when there is substantial variation in sire quality. Whether females invest more resources in the offspring of high-quality mates (differential allocation, DA) or in the offspring of low-quality mates (reproductive compensation, RC) is not consistent in the literature and both effects can be predicted by theoretical models. In the field cricket, Gryllus pennsylvanicus Burmeister, 1838 (Orthoptera: Gryllidae: Gryllinae), females are attracted more to calling songs of high-quality males than to those of low-quality males. We tested whether females invest reproductive resources differentially based on perceived mate quality. We manipulated female perception of male quality by allowing virgin females to approach a speaker broadcasting either high- or low-quality calling song (high or low calling effort respectively), and then mated them with a randomly chosen male that had been rendered incapable of calling. In the week following mating, females exposed to high-quality calling song gained less weight, laid more embryos, and laid larger embryos than females exposed to low-quality calling song, although only the first of these effects was statistically significant. These results support the DA hypothesis and suggest that females invest their reproductive output based on a trait (calling effort) that is an honest indicator of male quality.
differential allocation, Gryllus pennsylvanicus , mate choice, maternal effects, reproductive compensation, sexual selection
Mate choice can occur at various stages of mating (
Successful demonstration of differential investment requires careful manipulative experiments (
The study of differential investment by females has been dominated with avian examples (reviewed in
Male field crickets (Gryllidae: Gryllinae) produce both a long-range calling song used to attract females from a distance, and a short-range courtship song produced just prior to copulation (
In this study, we manipulated apparent mate quality as perceived by female fall field crickets, Gryllus pennsylvanicus Burmeister, 1838, by exposing virgin females to playbacks of either high or low effort calling songs, since greater calling effort is both preferred by females (
Late-instar G. pennsylvanicus nymphs were individually housed in plastic containers (9 cm diameter, 8 cm high) with several pieces of rabbit chow (Martin’s Little Friends Rabbit Food) for food, a cotton-plugged microfuge tube filled with water for moisture, and a small piece of cardboard egg carton for shelter. We measured body weight to the nearest milligram using a Mettler AE 50 balance on both the day following their moult to adulthood and the day prior to testing – the latter being used to match experimental pairs. The experiment had a paired design such that pairs of females, experiencing either the high- or low-effort song (see below), were matched for weight (within 5%) and were mated to one of a pair of males that were also matched for weight. In this way, we minimized variation in female reproductive output due to differences in female and male body size (which is linked to attractiveness, e.g.
Calling songs were recorded from wild males in Mississauga, Ontario (43°32‘50.51“N, 79°39‘37.80“W) in August and September of 2003. Songs were recorded using an Audio-Technica shotgun microphone connected to a Tascam DA-P1 digital audio tape recorder. Recordings were transferred to a computer, and saved as 48 kHz, 16-bit mono wav-files using CoolEdit 2000. Attractive and unattractive calling songs were the same as those used in
We allowed sexually mature (minimum of 10 days post adult eclosion; KAJ pers. obs.), virgin females to approach speakers broadcasting either attractive (HT) or unattractive (LT) calling song. We conducted no-choice phonotaxis trials in a sound-attenuating room to minimize environmental noise and under red light as crickets are nocturnal. The phonotaxis arena we used was identical to the one used by
After a female chose the broadcasting speaker, she was corralled on top of the speaker inside a plastic tube (7.5 cm diameter, 8 cm high). To re-acclimate the female, following this disruption, we allowed a further two-minute broadcast of the same calling song played during their phonotaxis trial. We then stopped the calling song and added an experimentally silenced male (see below) to the cylinder. Then we exposed all females to the same recording of a courtship song to induce the female to mate. We played the courtship song as soon as we observed the silenced male raising his truncated singing forewings. All males were isolated from the calling songs broadcast during the trials to reduce any possible effects the songs may have had on the male.
Prior to mating, males were experimentally silenced by trimming off the ends of the forewings with a pair of micro-scissors thereby removing the stridulatory apparatus necessary in song production (
Following spermatophore transfer, we restrained females for an hour, on the surface of a petri dish with a small piece of plastic wrap weighed down by a plastic ring. By restraining the female, we controlled for spermatophore attachment duration by preventing the female from eating or detaching the spermatophore, as females can control paternity through the removal of the spermatophore (
Following copulation, we provided females with moist gauze as an oviposition substrate, food, water, and shelter. At one-week intervals following mating, we weighed each female and collected all embryos laid during the week. We counted the embryos laid by each female and then subsampled a maximum of 10 embryos, which were then measured using ImageJ (Version 1.37). Embryo morphological measurements collected were: length, perimeter and area. Thus, for every week following the experiment until death we measured each female’s weight change, number of embryos laid, and embryo morphology.
Embryo measurements (length, perimeter and area) were reduced to a single measure of overall embryo size using a principal component analysis conducted in SPSS (Version 23). The mean value of all the embryos measured in each clutch (range 1 to 10 embryos measured) were included in the PCA, meaning that each clutch was represented by one length, perimeter and area measurement. Prior to statistical analysis, all data were tested for normality using Kolmogorov-Smirnov normality tests. As most dependent variables failed to satisfy the parametric assumption of normality, and sample size was reduced because several females failed to lay embryos, we chose to use randomization procedures to test our hypotheses. Specifically, we used permutation tests (
We assessed 31 pairs of females for their latency to respond to a male’s calling song (either high or low-quality), and then their subsequent reproductive output. Females in the two experimental groups (HT or LT) did not differ in weight before the treatment application (mean difference [LT – HT], 95% CI: 0.3 mg, -5.0–5.4 mg; N = 31 pairs, paired permutation test p = 0.918). All 62 females responded to the speaker broadcasting the calling song within the 20-minute time frame. Females responded more quickly to high- than low-quality calling songs (mean difference [LT – HT], 95% CI: 204.5 s, 44.8–368.7 s, N = 31 pairs, paired permutation test p = 0.023; Fig.
Following mating, eight individual females failed to lay embryos during their lifetime. There was no difference between females of either treatment in their likelihood of failing to produce embryos (LT: 5/29, HT: 3/29; Chi-Squared with continuity correction: χ2 = 0.144, p = 0.704). Because one female‘s failure to lay embryos would eliminate both females from a paired analysis, we decided to include all females who laid embryos at least once and conduct unpaired statistical analyses to maximize our sample size. Furthermore, one female died midway through the first week of embryo laying, which prevented us from measuring her weight change and so we eliminated her from subsequent analyses giving us a final sample size of 51 females (LT: n=25, HT: n=26).
To test for an effect of song exposure on female reproductive output, we compared the embryo laying rate, mass change, and embryo size of LT and HT females during: 1) the first week of embryo deposition (Week 1) – the most biologically relevant time period because few gryllids live beyond 25 days in the wild (
The principal components analysis of embryo length, area (square root) and perimeter resulted in one principal component with an eigenvalue over 1 that explained over 91% of the variation in embryo measurements (Table
Females exposed to high-quality song (HT) gained less weight, laid larger embryos and laid more embryos during the first week after mating than females exposed to low-quality song (LT). Only the effect on weight change was found to be statistically significant (mean difference [LT – HT], 95% CI: weight change = 57.9 mg, 20.4–96.9 mg, N = 51, permutation test p = 0.014, Fig.
Summary of the results of the principal components analysis of the three embryo measures. Values are the factor loadings and percent variance explained by principal component one.
Embryo Measure | PC1 |
---|---|
Area (square root) | 0.890 |
Perimeter | 0.935 |
Length | 0.918 |
% Variance Explained | 91.4 |
Female G. pennsylvanicus preferred (responded more quickly to) high-quality rather than low-quality calling songs (Fig.
Although modeling suggests that DA will be more prevalent than RC in nature (
Female body size is positively related to reproductive output in G. pennsylvanicus crickets (
We were unable to detect any statistically significant differences in oviposition rate and embryo morphology. It is possible that female G. pennsylvanicus use song quality to differentially invest in other fitness traits such as embryo weight, hatching success, nymphal hatching size, or sex ratio. Perhaps female crickets use their energy reserves to allocate a hormone or a chemical that increases offspring fitness, like that of birds, that was not explored in this study. For example, female zebra finches paired with attractive males (
Thank you to Glenn Morris for his advice on playback experiments and all things acoustic, Mark Fitzpatrick for his valuable insight and knowledge, as well as Jonathan Schneider for all his support and helpful suggestions. This research was funded by a Discovery Grant from the Natural Sciences and Engineering Research Council (NSERC) to DTG and an NSERC Post-Graduate Scholarship to KAJ.