Middle age females are most interested in mating: Lessons from a cricket

How age influences phonotaxis in virgin female Jamaican field crickets (Gryllus assimilis)

A new article in PeerJ written by Karen Pacheco, Jeff Dawson, Mike Jutting, and Sue Bertram

Click here for a copy of our PeerJ article

Click here for the Bertram Lab website

Female mate choice can heavily influence the evolution of male sexual signals. While mate choice was once thought to be a consistent and stable behaviour[1], research has shown mate selection is often very dynamic and variable throughout a female’s life. There are a number of environmental and internal factors that can affect a female’s mate choice (Figure 1). For instance, a female suddenly in danger of encountering a predator may alter her final mate decision[2]. A female’s past sexual experience[3] and her age[4] [5] [6] can also play a role in determining her mate choice. We currently have a vague understanding of how and why various intrinsic factors, such as female age, can cause variation in mate preferences and what the overall effect is on the evolutionary direction of male sexual traits.

Figure 1. Network of some of the intrinsic and extrinsic factors that could influence the final mate choice expressed before copulation; the interaction of these mate preference cues can drive sexual selection[7].

In one of our studies, which was recently published in PeerJ, we examined how one of these factors, female age, influenced female mate preferences in the Jamaican field cricket, Gryllus assimilis. Research on other species including cockroaches (Nauphoeta cinerea)⁶ and guppies (Poecilia reticulate)⁵ has revealed that as females age, their health and likelihood of future reproduction progressively declines. Because of this, older females may be less choosy in selecting mates compared to younger females who have higher reproductive potential.

Figure 2. A) A cricket tethered on top of the sphere (part of trackball). An optical sensor picks up the movements made by the trackball, which is rotated by the cricket walking. This information is collected on a computer system[10].

Figure 2. B) Female cricket tethered on top of our trackball via spring attached to magnet.

In crickets and other acoustic insects, females find and assess the attractiveness of potential mates using acoustic signals produced by the males of their species (termed ‘phonotaxis’)[8] [9]. We tested a wide range of female ages and assessed female phonotactic response to a male acoustic mate attraction signal using a specially built apparatus called a trackball. The trackball enables us to suspend a female over rotatable sphere and measure her movement associated with her attempt to move towards a speaker playing a male’s acoustic signal (Figure 2). Using the trackball and associated computer software, we measured how fast a female moved towards the speaker (velocity), how far she moved (total path length), and whether she generally seemed to be attempting to move towards the speaker (net vector score).

We found that female age influenced phonotaxis response: older females (13 days post adult moult) moved further and at higher velocities than females in other age groups in an attempt to reach the speaker (Figure 3).

Figure 3. How age affects female phonotaxis measures. Letters above each age reveal significant differences.

We also found that older females (10-13 days post adult moult) tended to more accurately orient themselves and move towards the active speaker than younger females (1-7 days post adult moult). The polar plots below (Figure 4) show the average direction and velocity (red arrows) towards the active speaker (0°) for females across all 10 age groups.

Figure 4. Polar plots indicating speed and direction moved for each age group tested. Inner circular gridlines indicate velocity magnitude (cm/s) and tic marks around the outside of the circle represent velocity angle. Red arrows show the mean velocity for all 20 females in each age group. The large, multi-colored plot shows the differences in average velocity across age groups.

Overall, we found age influenced female G. assimilis phonotaxis, where middle aged adult females’ (10-13 days old) displayed the strongest phonotaxis compared to younger or older females. The high speed and long distance travelled observed in young females (1-7 day) may signify higher energy reserves⁹, but their random orientation suggests little interest in the standardized acoustic mate attraction signal. We provide two possible explanations for the young females’ inattention towards the standard mate attraction signal: stronger preferences and lack of maturity. Very young females may have greater requirements in mate selection and prefer more extreme male traits[11]. Alternatively, very young females may be too young to respond to the call because they are not reproductively mature yet. Future research should present young females with multiple male signals to determine if indeed they are reproductively immature or only phonolocating toward signals with extreme trait values. Conversely, the older females oriented toward the speaker, suggesting interest, but walked at reduced speeds and covered shorter distances, possibly indicating senescence[12]. Overall, our findings are consistent with most studies on how age influences mating preference: diminished choosiness with increasing age[13] [14]. Our study suggests 10- and 13-day females are most responsive when quantifying the preference landscape for G. assimilis sexual signals.

Karen Pacheco is about to complete her MSc degree in Biology at Carleton University

Karen Pacheco, Jeff Dawson, Mike Jutting, and Sue Bertram (2013). How age influences phonotaxis in virgin female Jamaican field crickets (Gryllus assimilis) PeerJ : 10.7717/peerj.130

[1] Andersson, M. 1994. Sexual Selection. Princeton: Princeton University Press.

[2] Magnhagen, C. 1991. Predation risk as a cost of reproduction. Trends in Ecology & Evolution, 6, 183-186.

[3] Dugatkin, L.A. 1992. Sexual selection and imitation: females copy the mate choice of others. The American Naturalist, 139, 1384-1389.

[4] Jouventin, P., LeQuette, B., & Dobson, F.S. 1999. Age-related mate choice in the wandering albatross. Animal Behaviour, 57, 1099-1106.

[5] Kodric-Brown, A., & Nicoletto, P.F. 2001. Age and experience affect female choice in the guppy (Poecilia reticulata). The American Naturalist, 157, 316-23.

[6] Moore, P.J., & Moore, A.J. 2001. Reproductive aging and mating: The ticking of the biological clock in female cockroaches. Proceedings of the National Academy of Sciences, 98, 9171-9176.

[7] Widemo, F., & Sæther, S. A. 1999. Beauty is in the eye of the beholder: causes and consequences of variation in mating preferences. Trends in Ecology and Evolution, 14, 26-31.

[8] Solymar, B., & Cade, W.H. 1990. Age of first mating in field crickets Gryllus integer (Orthoptern: Gryllidae). The Florida Entomologist, 73, 193-195.

[9] Prosser, M.R. 1994. Effect of Age On Female Choice in the Field Cricket, Gryllus integer. Unpublished Masters thesis, Brock University, St. Catharines, Ontario.

[10] Hedwig, B. & Poulet, J.F. 2004. Complex auditory behaviour emerges from simple reactive steering. Nature, 430, 781-785.

[11] Ryan, M.J., Keddy-Hector, A. 1992. Directional patterns of female mate choice and the role of sensory biases. The American Naturalist, 139, 4-35.

[12] Prosser, M.R., Murray, A.M., & Cade, W.H. 1997. The influence of female age on phonotaxis during single and multiple song presentations in the field cricket, Gryllus integer (Orthoptera: Gryllidae). Journal of Insect Behavior, 10, 437-449.

[13] Roff, D.A. 1992. The evolution of life histories: theory and analysis. London: Chapman & Hall.

[14] Mautz, B.S., & Sakaluk, S.K. 2008. The effect of age and previous mating experience on pre- and post-copulatory mate choice in female house crickets (Acheta domesticus L). Journal of Insect Behavior, 21, 203-212.

Adaptive Plasticity in Wild Field Crickets’ Acoustic Signaling

A new article in PLOS ONE written by

Susan Bertram, Sarah Harrison, Ian Thomson, and Lauren Fitzsimmons

Click here for a copy of our PLOS ONE article

Click here for the Bertram Lab website

Figure 1: Changes to the density of competitors is an example of environmental variability commonly faced by organisms in the wild.

Environmental change is a common obstacle that animals have to overcome. Temporal or spatial changes in the weather, food availability, predator density, mate availability, or competitor density are just some examples of the environmental variability commonly faced by animals in the wild (Figure 1).The optimal phenotype (an organism’s morphology, physiology, behavior etc.) for a given environment often changes as environmental conditions change. For example, a caterpillar feeding on oak flowers will develop into a mimic of an oak catkin, while a sibling caterpillar feeding on leaves will develop into a mimic of a twig (Figure 2). These caterpillars may avoid predation by camouflaging themselves to match their environments.

Figure 2: Nemoria arizonaria caterpillars: (a) summer broods feed on oak leaves and
Develop to resemble oak twigs, (b) while spring broods feed on and resemble oak catkins (Whitman and Agrawal 2009).

Figure 3: Hydrangea macrophylla flowers grown in acidic soil produces blue flowers, while flowers grown in neutral or alkaline soil produce pink flowers.

If individuals are unable to adapt to changes in their surroundings, they may experience reduced survival or reproductive success compared to individuals who are able to adapt.Phenotypic plasticity is the ability to change behaviour, appearance, or other characteristics in response to environmental change. For instance, Hydrangea macrophylla produce either blue or pink flowers depending on soil alkalinity (Figure 3). Phenotypic plasticity may be adaptive as long as environmental variation is predictable and the benefits of plasticity outweigh the costs. For instance, phenotypic plasticity in sexually selected traits may be particularly adaptive if there are frequent predictable changes to the socio-sexual environment (e.g. fluctuation in mate density).

In our study, recently published in PLOS ONE, we examined the phenotypic plasticity of male field crickets’ sexually selected acoustic signals for two species: the fall field cricket, Gryllus pennsylvanicus and the spring field cricket, G. veletis (Figure 4).

Figure 4: The fall field cricket (Left- G. pennsylvanicus male) and the spring field cricket (Right- G. veletis male) are both found throughout North America.

Male crickets produce acoustic signals by raising their forewings and rubbing them together, each closing stroke producing a pulse of sound with 3-4 pulses grouped into a chirp (Figure 5). These acoustic calls are used to attract females, and females choose mates on the basis of the quantity and fine-scale structure of these signals. Female movement and sexual receptivity in the wild often follows predictable fluctuations throughout the day (diel rhythms), which may partially be explained by hourly fluctuations in the biotic (predator and parasite density) and abiotic (light and temperature levels) environment. Therefore, males that synchronize their daily signalling rhythms to match female mating activity are likely to have higher reproductive success. Here we examined how male acoustic signalling in the laboratory changes over the course of the day and compared this to the known reports of diel rhythms in female mating activity in the wild.
We captured wild males and brought them to our laboratory at Carleton University where we recorded their acoustic signalling for 2-4 days. We found that both spring and fall field crickets exhibited phenotypically plastic signalling behavior, with most males signalling more often and more attractively during the time of day when female mating activity is the highest in the wild (fall field cricket: night time and early morning; spring field cricket: early morning and afternoon). Most male crickets (from both species) chirped more often during the time of the day that female mating activity is highest in the wild (Figure 5). However, a few males of each species signalled in a seemingly maladaptive manner during times when female mating activity is lowest in the wild. Diel rhythms in signalling also differed across species, which may be beneficial in preventing lethal hybridization when spring and fall field crickets overlap temporally and spatially in mid-summer.

Figure 4: Waveforms of long-distance mate attraction signals of one G. pennsylvanicus and one G. veletis male. Figures show typical long-distance mate attraction signal for each species and how signaling typically changes during time periods indicative of low (A & B) and high (C & D) mating activity in the wild. Signal fine-scale properties are indicated as follows: ChD = chirp duration; IChD= interchirp duration; PPCh = pulses per chirp; PD = pulse duration; IPD = interpulse duration; and PP = pulse period, which combines PD and IPD.

Overall, our findings suggest that male field crickets exhibit phenotypically plastic mate attraction signals and that diel rhythms in these signals are synchronized so that they are in phase with diel rhythms in female mating activity, suggesting that signalling plasticity may be adaptive. We have yet to determine how the costs and benefits of the phenotypic plasticity we observed in our species of field cricket ultimate affect fitness.

References:

Whitman, D. W. and A. A. Agrawal. What is Phenotypic Plasticity and why is it Important? Pages 1-63 in: D. W. Whitman and T. N. Ananthakrishna (editors), Phenotypic plasticity of insects: Mechanisms and consequences. Science Publishers, Inc, Enfield, NH

Related articles

• Quantitative Assessment of the Importance of Phenotypic Plasticity in Adaptation to Climate Change in Wild Bird Populations (plosbiology.org)
• Male crickets change their behaviour when watched by an audience (labchirps.wordpress.com)