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Michael D. Greenfield

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Michael D. Greenfield Animal Choruses Emerge from Receiver Psychology (A Tale of Two Synchronies) Michael D. Greenfield Univ. St. Étienne (ENES), France Univ. Kansas (Ecol & Evol Biol), USA Labex CeMEB Mediterranean Center for Environment and Biodiversity What is an animal chorus ? (It’s about time) Temporal adjustments in broadcasting at three levels of precision : a b (an evening chorus) c d individual e 12 18 24 6 12 h - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - - (collective singing * leader - - - - - - - - - - - - - - - - - - - - - - - - - - - - bouts) - - - - - - - - - - - - - - - - - - - - - - 0 5 10 15 min 90° phase angle (regular rhythm - - - - - - and precise phase - - - - - - relationships) 0 1 2 3 sec 0 5 10 Time (sec) Physalaemus pustulosus (Túngara frog; Anura: Leptodactylidae); 5 Male Chorus Physalaemus pustulosus (Túngara frog; Anura: Leptodactylidae); 5 Male Chorus A B C Individual D E -2 0 2 4 6 8 10 Time (sec) Frogs have rules + - 0 15 30 45 60 Time (sec) Magicicada cassini (Cicadidae); Periodical Cicada (17-year) Synchronous Chorus; Brood IV; June 1998; Douglas Co., Kansas Pteroptyx tener (Lampyridae); Synchronous fireflies of the Indo-Malayan Region Kumari Nallabumar 2002 Strogatz & Stewart 1993 Uca annulipes (Crustacea: Ocypodidae); Western Indo-Pacific; Synchronized waving Stefano Cannicci Synchronized courtship in fiddler crabs; Backwell et al. 1998 Utetheisa ornatrix (Lepidoptera : Arctiidae) Specialized rhythmic chorusing : potential adaptive features * Retention of species-specific rhythm or call envelope -- -- -- -- -- -- -- -- -- -- -- -- -- -- -- -- -- -- -- -- * Evasion of predators ; detection of predators Time → * Maximization of collective signal intensity of local group * Unmasking of sexually-selected signal characters ; -- -- -- -- ability to detect and evaluate rivals -- -- -- (Greenfield 2005) Alternative to the adaptationist paradigm : (the null hypothesis) Choruses might also arise simply as an ‘emergent property’ of local interactions between singing neighbors. That is, the overall chorus structure per se, even when very complex and seemingly specialized, is neutral in terms of preference by female receivers and the benefits that male signalers might accrue from generating it. (Greenfield & Schul 2008 ; Greenfield 2015) How might this work ? 3-step pathway : Collective singing patterns in choruses simply emerge from the ‘receiver psychology’ of female perception and preference. 1) Females ignore male calls that follow a neighbor’s by a brief interval. 2) Males adjust call rhythm (phase) upon hearing a stimulus or neighbor. 3) When multiple males use equivalent adjustments an expansive chorus of synchrony and/or alternation may arise. Importantly, the display can be generated in the absence of any selection expressly favoring synchrony or alternation. Loudspeaker 14 12 1 - - - - - - - 10 8 2 -- -- -- -- -- -- 6 400 msec 4 Number Females 2 0 1 - 27.5 55.0 O + -- PulseSong Length (msec) 2 Neoconocephalus spiza (Orthoptera : Tettigoniidae) : female preference for song length Phonotaxis 1 - Phase angle O + -- 2 1 - 24º 12 Neoconocephalus spiza : 12 female preference for 24º leading song overrides 1 song length 0 100 200 Time (msec) Phase Angle -180° - - 1.0 -- -- 0.8 -81° - - -- -- 0.6 0.4 -54° - - -- -- 0.2 -24° - - Preference for long chirp long for Preference 0.0 -- -- -200 -150 -100 -50 0 50 100 150 200 o 0° - - Phase Angle ( ) -- -- Greenfield & Roizen 1993 24° - - 1 - -- -- O + 180° - - -- 2 -- -- 400 msec Neoconocephalus spiza - precedence effect in female phonotaxis Monte Carlo Simulation Response phase, Monte Carlo Simulation Response phase, {(T' - T) / T} • 360° InhibitoryPRC slope Resetting = s : {(T' - T) / T} • 360° InhibitoryPRC slope Resetting = s : TT TT´ TT FocalFocal AnimalAnimal StimulusStimulus dd or Neighbor or Neighbor Time StimulusStimulus phase, phase, Time (d(d / /T) T) • •360360°° tt rr Phase Response Curve (PRC) Oscillator level Oscillator level 180° ' StimulusStimulus Phase Phase = = (d (d / /T) T) • • 360360°° Greenfield et al. 19971997 BasicBasic model model : : TT´ ´== (T (T + + ε )εResponse )+Response + (s (s • •d),d), Phase Phase where where = = ε {(T ε{(Tisis´´ - - a T)aT) stochastic/ stochastic /T T } } • • 360360°° elementelement 0° FullFull model model : : Response Phase ' TT´ ´== (T (T + + ε )ε )+ + s{(d s{(d + + l l/ /v) v) - -(r(r - -t)}t)} + + (y (y --x)x) 0° 180° Stimulus Phase y (msec) _____ Neoconocephalus spiza ____ (Tettigoniidae) : ___ __ PRC intercepts adjusted by _ stimulus length Response Phase Response Stimulus Phase Greenfield & Roizen 1993 Monte Carlo Simulation Response phase, {(T' - T) / T} • 360Response° PRC phase, slope = s {(T' - T) / T} • 360° PRC slope = s Monte Carlo Simulation Response phase, T T´ T {(T ' - T) / T} • 360° PRC slope = s Focal Animal T T´ T d Stimulus Focal Animal or Neighbor Stimulus phase, Stimulus Time d Stimulus phase, (d / T) • 360° or Neighbor Stimulus(d / T) • 360 phase,° t Time (d / T) • 360° t r Oscillator level r Oscillator level Greenfield et al. 1997 Basic model Basic: model : Greenfield et al. 1997 Basic model : T´ = (T + ε) + T(s´ =• d),(T + ε) where + (s • d), ε is where a stochastic ε is a stochastic element element T´ = (T + ε) + (s • d), where ε is a stochastic element Full model : Full model : Full model : T´ = (T + ε) + Ts{(d´ = (T + +l /ε) v) + - s{(d(r - t)}+ l +/ v) (y - -(rx) - t)} + (y - x) T´ = (T + ε) + s{(d + l / v) - (r - t)} + (y - x) Greenfield, Tourtellot & Snedden 1997 Monte Carlo Simulation Michael Tourtellot VisualBASIC® Maestro Monte Carlo Simulation Spacing ; 2 males separated by 5 m ; 1 female Calls of the 2 males ; mostly synchronized Male song adjustment parameters Monte Carlo Simulation : Alternation Synchrony Greenfield et al. 1997 Male A x Neoconocephalus spiza (Tettigoniidae: Conocephalinae); Central America; (imperfect) synchrony x B Time (sec) 3-step pathway : Collective singing patterns in choruses simply emerge from the ‘receiver psychology’ of female perception and preference. 1) Females ignore male calls that follow + a neighbor’s by a brief interval. No experimental evidence for coevolution between male and female traits ? 2) Males adjust call rhythm (phase) + upon hearing a stimulus or neighbor. 3) When multiple males use equivalent adjustments an expansive chorus of synchrony and/or alternation may arise. Importantly, the display can be generated in the absence of any selection expressly favoring synchrony or alternation. Question 1 : Did male song adjustment (inhibitory resetting) coevolve with female response to relative call timing (leading vs. following calls) ? Tettigoniidae ; Bradyporinae A B Ephippiger diurnus C Alternation + Synchrony individual alt D D B alt syn 3 m C 5 s Females ignore following calls ; Flightless ; negligible dispersal ; Male song adjustment (inhibitory resetting) ; narrow habitat preference ; Chorusing (alternation and synchrony) isolated, genetically differentiated populations Ephippiger diurnus (Tettigoniidae) Flightless ; negligible dispersal ; narrow habitat preference ; geographically isolated, genetically differentiated populations → 31 34 Application of comparative 65 09 11 phylogenetic methods possible 66 ‘Comparative Method’ ; 17 E. diurnus populations ‘sampled’ ; Phylogenetic analysis indicates branching topology ; Mitochondrial (COI) data ; Best-fitting nucleotide substitution model Clade 2 ʘ 7 Clade 1 Measurement of female follower leader perceptual trait Col de Chioula 0.5 Col de Chioula population 0.4 f for leader * * * 0.3 0.2 f – maximum separation leader preference at which females ignore † follower 0.1 follower delay 0.0 Index of Index 30 150 400 600 900 1200 time Leader – follower call separation (ms) Measurement of male song t T peak adjustment trait rb basal r Time → T ′ T ′ level Oscillator Oscillator 1 T ′2 3 focal male rb rb rb 1 2 3 stimulus d1 d3 m m – minimum delay before male resumes singing 10 600 ms bin ms - Col de Chioula - Male # 37 Col de Chioula 500 8 (ms) m Col de Chioula 400 6 population Focal male does delay 300 Calls per 50 per Calls not call during 4 post-stimulus interval 200 2 100 Synthetic song 0 minimum ; m 0 stimulus at t = 0 0 200 400 600 800 1000 29 30 33 34 36 37 50 51 Post-stimulus call delay (ms) Male # Predictions : If male song adjustments have coevolved with female perception, m should be ≥ f such that males do not broadcast ineffective following calls. Moreover, if m ≈ f, males will maximize their call rate while at the same time Populations: 1) Mireval, 2) Vias, 3) Peyriac de Mer, 4) Feuilla, 5) Col de Mantet, forgoing the broadcast of following calls. 6) Font Romeu, 7) Latour de Carol, 8) Col de Puymorens, 9) Hospitalet près l’Andorre, 10) Mérens-les-Vals, 11) Col de Chioula, 12) Carcanières, 13) Port de Lers, 14) Vilamòs, 15) Cigalère, 16) Le Lioran, 17) Pouzol. Col de Puymorens ; 8 Hospitalet près l’Andorre ; 9 Female precedence effect ; Maximum delay (msec) at which leading calls are preferred. Male phase adjustment ; Minimum delay (msec) before singing after a stimulus or neighbor. A For the 17 populations sampled, m ≈ f . B 2500 2000 1500 ρ = 0.87 1000 ; minimum delay (ms) ; minimum delay m 500 Populations: 1) Mireval, 2) Vias, 3) Peyriac de Mer, 4) Feuilla, 5) Col de Mantet, 6) Font Romeu, 7) Latour de Carol, 8) Col de Puymorens, 9) Hospitalet près l’Andorre, 10) Mérens-les-Vals, 11) Col de Chioula, 12) Carcanières, 13) Port de Lers, 14) Vilamòs, 15) Cigalère, 16) Le Lioran, 17) Pouzol. 0 0 500 1000 1500 2000 2500 f ; maximum separation (ms) Is the m – f correlation
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