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Adult acoustic experience
influences reproductive behavior
more than does juvenile
experience in female field crickets
Elizabeth Swanger, Marlene Zuk
University of Minnesota
Graduate Program in Ecology, Evolution, and
Behavior
swang009@umn.edu
August 5, 2014
miracleofnature.org
Greg Rhodes
Alexander Wild
slenderocean on Flickr
miracleofnature.org
BRIGHTER BIGGER
FASTER LOUDER
less bright smaller
slower quieter
Jennions & Petrie 1997, Biol Rev 72: 283
The social environment
influences mating behavior
Kasumovic & Brooks 2011, Quart Rev Biol 83: 181. Fowler-Finn & Rodriguez 2011, J Evol Biol 66: 459.
Females often attend to the quantity and
attractiveness of signaling males and adjust their
mating thresholds and preferences accordingly.
Social environment, mate choice
plasticity, and selection
selection
social
environment
responses
to sexual
signals
Timescale of phenotypic
plasticity
Bill Hubick; Wikimedia Commons; Michael Hrabar
1Marler 1970. J Comp Phys Psych Monogr 71: 1. 2Sheehan & Tibbetts 2011. Science 334: 1272.
CRITICAL WINDOW1 FIXED DURING
DEVELOPMENT
FLEXIBLE THROUGHOUT
ADULTHOOD2
Social environment, mate choice
plasticity, and selection
Is reproductive behavior fixed based on
experiences during development?
Does it remain flexible throughout adulthood?
What are the relative roles of the juvenile and adult
social environments in adult females’ responses to
sexual signals?
The Pacific field cricket
(Teleogryllus oceanicus)
Tinghitella et al. 2011. J Evol Biol 24: 1199.
Acoustic sexual signals in T.
oceanicus
Zuk et al. 2008. Anim Behav 76: 1065.
CALLING SONG
Long-distance attractor
Long chirp followed by
short chirps
COURTSHIP SONG
Short-range
More variable, long and
short chirps
Females accept or reject
Social experience during
development and adulthood
http://www.sardi.sa.gov.au/
Juvenile experience influences
responses to sexual signals
Bailey & Zuk 2008. Proc B 275: 1651.
♬♪♫♫
Mating experience influences
responses to subsequent mates
Rebar et al. 2011. Behav Ecol 22: 303.
Females previously mated to males with nonpreferred
courtship songs exhibit stronger preferences in favor of their
next mate, regardless of his attractiveness.
Time to remate (1/t)
Spermatophore
retention (min)
Juvenile acoustic experience
influences responses to signals
Mating experience influences
responses to subsequent mates
WHEN DOES SOCIAL
EXPERIENCE MATTER MORE?
Factorial design:
Stage x acoustic environment
Song Song
No Song Song
Song No Song
No Song No Song
Juvenile
environment
Adult
environment Responsiveness to calling song
♬
♬
♬
♬
Factorial design:
Stage x acoustic environment
Song Song
No Song Song
Song No Song
No Song No Song
Juvenile
environment
Adult
environment Responsiveness to calling song
♬
♬
♬
♬
Factorial design:
Stage x acoustic environment
Song Song
No Song Song
Song No Song
No Song No Song
Juvenile
environment
Adult
environment Responsiveness to calling song
♬
♬
♬
♬
Adult exposure to song reduces
contact with speaker
Adult environment:
p = 0.001
Juvenile environment:
p = 0.07
Juvenile Environment:
No Song
Juvenile Environment:
Song
Adult song exposure increases
time to contact speaker
Juvenile Environment:
No Song
Adult environment:
p = 0.046
Juvenile environment:
p > 0.20
Juvenile Environment:
Song
Adult song exposure increases
distance settled from speaker
Juvenile Environment:
No Song
Juvenile Environment:
Song
Adult environment:
p = 0.024
Juvenile environment:
p > 0.70
What is the timescale of plasticity
in reproductive behavior?
Pet Solutions Pet Care Corner; Brian Robin
What are the relative roles of juvenile and adult
social experience in determining female
responses to sexual signals?
Behavioral shifts should track
demographic shifts
Time (days)
1 2 3 4 5 6 7 8 9 10
BJSmit on Flickr; miracleofnature.org
Social environment, mate choice
plasticity, and selection
selection
social
environment
responses
to sexual
signals
Plasticity in mating behavior may
have facilitated rapid evolution
Wikimedia Commons, Nathan Bailey
selection
social
environment
responses
to sexual
signals
Plasticity in mating behavior may
have facilitated rapid evolution
Kauai
Hawaii
Maui
Molokai
Oahu
>90%
~0-10%
~50%
How ELSE does behavior
influence evolution?
Roaming Romeos:
evolution in silence
selects for male crickets
with increased exploratory
behaviors.
Dr. Susan Balenger
Assembly Hall
12:20-12:40
THANK YOU!
Committee: Mark Bee, Emilie Snell-Rood,
Marla Spivak, Dave Stephens
Zuk Lab: Susan Balenger, Beth Bastiaans,
Justa Heinen-Kay, and small horde of
undergrads, especially Patrick O’Hare and
Paul Swim
UMN Graduate Program in Ecology,
Evolution, and Behavior especially Sarah
Jaumann, Virginia Heinen, and Mike Wells
Friends and Family
You!
Funding Sources:

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Insect love songs: how the social environment influences mating behavior

  • 1. Adult acoustic experience influences reproductive behavior more than does juvenile experience in female field crickets Elizabeth Swanger, Marlene Zuk University of Minnesota Graduate Program in Ecology, Evolution, and Behavior swang009@umn.edu August 5, 2014
  • 2. miracleofnature.org Greg Rhodes Alexander Wild slenderocean on Flickr miracleofnature.org BRIGHTER BIGGER FASTER LOUDER less bright smaller slower quieter Jennions & Petrie 1997, Biol Rev 72: 283
  • 3. The social environment influences mating behavior Kasumovic & Brooks 2011, Quart Rev Biol 83: 181. Fowler-Finn & Rodriguez 2011, J Evol Biol 66: 459. Females often attend to the quantity and attractiveness of signaling males and adjust their mating thresholds and preferences accordingly.
  • 4. Social environment, mate choice plasticity, and selection selection social environment responses to sexual signals
  • 5. Timescale of phenotypic plasticity Bill Hubick; Wikimedia Commons; Michael Hrabar 1Marler 1970. J Comp Phys Psych Monogr 71: 1. 2Sheehan & Tibbetts 2011. Science 334: 1272. CRITICAL WINDOW1 FIXED DURING DEVELOPMENT FLEXIBLE THROUGHOUT ADULTHOOD2
  • 6. Social environment, mate choice plasticity, and selection Is reproductive behavior fixed based on experiences during development? Does it remain flexible throughout adulthood? What are the relative roles of the juvenile and adult social environments in adult females’ responses to sexual signals?
  • 7. The Pacific field cricket (Teleogryllus oceanicus) Tinghitella et al. 2011. J Evol Biol 24: 1199.
  • 8. Acoustic sexual signals in T. oceanicus Zuk et al. 2008. Anim Behav 76: 1065. CALLING SONG Long-distance attractor Long chirp followed by short chirps COURTSHIP SONG Short-range More variable, long and short chirps Females accept or reject
  • 9. Social experience during development and adulthood http://www.sardi.sa.gov.au/
  • 10. Juvenile experience influences responses to sexual signals Bailey & Zuk 2008. Proc B 275: 1651. ♬♪♫♫
  • 11. Mating experience influences responses to subsequent mates Rebar et al. 2011. Behav Ecol 22: 303. Females previously mated to males with nonpreferred courtship songs exhibit stronger preferences in favor of their next mate, regardless of his attractiveness. Time to remate (1/t) Spermatophore retention (min)
  • 12. Juvenile acoustic experience influences responses to signals Mating experience influences responses to subsequent mates WHEN DOES SOCIAL EXPERIENCE MATTER MORE?
  • 13. Factorial design: Stage x acoustic environment Song Song No Song Song Song No Song No Song No Song Juvenile environment Adult environment Responsiveness to calling song ♬ ♬ ♬ ♬
  • 14. Factorial design: Stage x acoustic environment Song Song No Song Song Song No Song No Song No Song Juvenile environment Adult environment Responsiveness to calling song ♬ ♬ ♬ ♬
  • 15. Factorial design: Stage x acoustic environment Song Song No Song Song Song No Song No Song No Song Juvenile environment Adult environment Responsiveness to calling song ♬ ♬ ♬ ♬
  • 16. Adult exposure to song reduces contact with speaker Adult environment: p = 0.001 Juvenile environment: p = 0.07 Juvenile Environment: No Song Juvenile Environment: Song
  • 17. Adult song exposure increases time to contact speaker Juvenile Environment: No Song Adult environment: p = 0.046 Juvenile environment: p > 0.20 Juvenile Environment: Song
  • 18. Adult song exposure increases distance settled from speaker Juvenile Environment: No Song Juvenile Environment: Song Adult environment: p = 0.024 Juvenile environment: p > 0.70
  • 19. What is the timescale of plasticity in reproductive behavior? Pet Solutions Pet Care Corner; Brian Robin What are the relative roles of juvenile and adult social experience in determining female responses to sexual signals?
  • 20. Behavioral shifts should track demographic shifts Time (days) 1 2 3 4 5 6 7 8 9 10 BJSmit on Flickr; miracleofnature.org
  • 21. Social environment, mate choice plasticity, and selection selection social environment responses to sexual signals
  • 22. Plasticity in mating behavior may have facilitated rapid evolution Wikimedia Commons, Nathan Bailey selection social environment responses to sexual signals
  • 23. Plasticity in mating behavior may have facilitated rapid evolution Kauai Hawaii Maui Molokai Oahu >90% ~0-10% ~50%
  • 24. How ELSE does behavior influence evolution? Roaming Romeos: evolution in silence selects for male crickets with increased exploratory behaviors. Dr. Susan Balenger Assembly Hall 12:20-12:40
  • 25. THANK YOU! Committee: Mark Bee, Emilie Snell-Rood, Marla Spivak, Dave Stephens Zuk Lab: Susan Balenger, Beth Bastiaans, Justa Heinen-Kay, and small horde of undergrads, especially Patrick O’Hare and Paul Swim UMN Graduate Program in Ecology, Evolution, and Behavior especially Sarah Jaumann, Virginia Heinen, and Mike Wells Friends and Family You! Funding Sources:

Editor's Notes

  1. Mate choice is really common in nature and is major component of sexual selection. Some individuals, usually females, preferentially mate with the most ornamented members of the opposite sex, usually males. While females of a species tend to agree on preferring more ornamented—brighter, bigger, faster signaling, or louder—individuals, there’s still variation. Some females still mate with males that are less bright, smaller, and signal slower or quieter. Females can vary in their choice behavior for a lot of reasons, but I’m particularly interested in how they use their social environment to decide who to mate with.
  2. One of the ways females can tell who is in their social environment is to attend to the sexual signals they can perceive around them. When sexual signals propagate over some medium, like vibrational or acoustic signals, the quantity and attractiveness of those signals tell females something about the quantity and attractiveness of the males they might mate with.
  3. The effects of the social environment produce a cool feedback loop: the strength and direction of selection influence the composition of the social environment, which influences female responses to male signals, which then determine what selection on those same signals looks like. For this study, I’m focusing on how the social environment influences individual females’ responses to sexual signals.
  4. A key component of plastic phenotypes is the timescale on which they are plastic. Some traits, like song learning in many birds, become fixed based on experience during critical windows in juvenile development. Males and females learn their songs and preferences, respectively, based on what they hear around them during this critical window. Similarly, the size of many insects is fixed once they reach adulthood, but for physical limitations: if you have an exoskeleton, you don’t get to grow anymore. Other traits, in contrast, can remain flexible throughout adulthood: adult female Polistes fuscatus paper wasps learn the faces of nestmates (as opposed to strangers) and adjust their aggressive behavior accordingly.
  5. So with this study, I looked at three related questions: is reproductive behavior fixed based on experiences during development? Or does it remain flexible throughout adulthood? Or if experiences during both stages are important in determining female behavior, what are their relative roles?
  6. I looked at these questions in the Pacific field cricket, Teleogryllus oceanicus, which is native to Australia and throughout the Pacific. It was introduced by human activity to Hawaii, where I work.
  7. T. oceanicus males sing two distinct songs: one is a long-distance calling song that attracts females from long distances and consists of a long chirp followed by series of short chirps. Once they’ve made contact with a female, they sing a short-range courtship song that is also composed of long and short chirps, but is more variable. Females can accept or reject males at this stage.
  8. So we already know adult females have functional ears, allowing them to perceive and localize male calling songs. But T. oceanicus undergoes an extended period of development and possesses functioning ears for the last few larval instars. This means they have an opportunity to perceive and assess their social environment prior to actually making mating decisions.
  9. T. oceanicus females vary in their mating behavior based on social experiences, both during rearing and adulthood. Let’s say this female on top was reared in the presence of calling song, which simulates a social environment full of males. The female on the bottom was reared in silence, simulating a scarcity of mates. If you presence both females with an attractive male song, they beeline for it. But if you present them with an unattractive male song, the female reared in silence beelines, but the female reared in the presence of song is slower to approach.
  10. Mating experience,
  11. Call: glm(formula = crickets$ResponseType ~ A_Env * J_Env + crickets$Courtship, family = binomial) Deviance Residuals: Min 1Q Median 3Q Max -1.8391 -1.1502 0.6826 0.9039 1.3569 Coefficients: Estimate Std. Error z value Pr(>|z|) (Intercept) -0.014639 0.296429 -0.049 0.96061 A_Envsong 1.364480 0.428368 3.185 0.00145 ** J_Envsong 0.723738 0.400879 1.805 0.07102 . crickets$Courtship -0.009951 0.009216 -1.080 0.28026 A_Envsong:J_Envsong -0.586167 0.624435 -0.939 0.34788 --- Signif. codes: 0 ‘***’ 0.001 ‘**’ 0.01 ‘*’ 0.05 ‘.’ 0.1 ‘ ’ 1 (Dispersion parameter for binomial family taken to be 1) Null deviance: 266.72 on 210 degrees of freedom Residual deviance: 250.15 on 206 degrees of freedom AIC: 260.15 Number of Fisher Scoring iterations: 4
  12. Anova Table (Type II tests) Response: TimeDiff_s Sum Sq Df F value Pr(>F) A_Env 14905 1 4.1570 0.04566 * J_Env 5225 1 1.4574 0.23186 crickets$Courtship 5371 1 1.4980 0.22554 A_Env:J_Env 39 1 0.0108 0.91748 Residuals 225884 63 --- Signif. codes: 0 ‘***’ 0.001 ‘**’ 0.01 ‘*’ 0.05 ‘.’ 0.1 ‘ ’ 1
  13. Anova Table (Type II tests) Response: crickets$Distance_cm Sum Sq Df F value Pr(>F) A_Env 10178 1 5.1888 0.02428 * J_Env 186 1 0.0948 0.75867 crickets$Courtship 1576 1 0.8033 0.37167 A_Env:J_Env 1039 1 0.5296 0.46800 Residuals 268733 137 --- Signif. codes: 0 ‘***’ 0.001 ‘**’ 0.01 ‘*’ 0.05 ‘.’ 0.1 ‘ ’ 1
  14. The effects of the social environment produce a cool feedback loop: the strength and direction of selection influence the composition of the social environment, which influences female responses to male signals, which then determine what selection on those same signals looks like. For this study, I’m focusing on how the social environment influences individual females’ responses to sexual signals.