Drop dead! Female mate avoidance in an explosively breeding frog

This is a sel -a chi ed e sion o an o iginal a icle. This e sion may di e om he o iginal in pagina ion and ypog aphic de ails. Au ho (s): Ti le: Yea : Ve sion: Copy igh : Righ s: Righ s u l: Please ci e he o iginal e sion: CC BY 4.0 h ps://c ea i ecommons.o g/licenses/by/4.0/ D op dead! Female ma e a oidance in an explosi ely b eeding og © 2023 The Au ho s. Published by he Royal Socie y Published e sion Di ich, Ca olin; Rödel, Ma k-Oli e Di ich, C., & Rödel, M.-O. (2023). D op dead! Female ma e a oidance in an explosi ely b eeding og. Royal Socie y Open Science, 10(10), A icle 230742. h ps://doi.o g/10.1098/ sos.230742 2023 oyalsocie ypublishing.o g/jou nal/ sos Resea ch Ci e his a icle: Di ich C, Rödel M-O. 2023 D op dead! Female ma e a oidance in an explosi ely b eeding og. R. Soc. Open Sci. 10: 230742. h ps://doi.o g/10.1098/ sos.230742 Recei ed: 30 May 2023 Accep ed: 21 Sep embe 2023 Subjec Ca ego y: O ganismal and e olu iona y biology Subjec A eas: beha iou /e olu ion/ecology Keywo ds: dea h eigning, Eu opean common og, expe ience, sexual con lic , hana osis, onic immobili y Au ho o co espondence: Ca olin Di ich e-mail: [email p o ec ed] Elec onic supplemen a y ma e ial is a ailable online a h ps://doi.o g/10.6084/m9. igsha e.c. 6858610. D op dead! Female ma e a oidance in an explosi ely b eeding og Ca olin Di ich 1,2,3 and Ma k-Oli e Rödel 1,3 1 Museum ü Na u kunde Be lin, Leibniz Ins i u e o E olu ion and Biodi e si y Science, In alidens aße 43, 10115 Be lin, Deu schland 2 Depa men o Biology and En i onmen al Sciences, Uni e si y o Jy äskylä, Jy äskylä, Finland 3 Be lin–B andenbu g Ins i u e o Ad anced Biodi e si y Resea ch (BBIB), Be lin, Ge many CD, 0000-0002-4447-4481; M-OR, 0000-0002-1666-195X Males’and emales’ ep oduc i e s a egies may di e , po en ially leading o sexual con lic . Inc eased e o s by males (ha assmen , o ced copula ion, in imida ion) o gain access o emales could e en nega i ely a ec emale su i al and hus lead o ep oduc i e ailu e o bo h indi iduals. In anu ans, a highe mo ali y isk o ma ing emales has been epo ed in explosi e b eeding species. Du ing hese ma ing e en s, se e al males cling o a emale, which a e mos ly unable o ge id o he unwan ed males. This can lead o he emale’s dea h. F om he li e a u e, i seems ha emales o explosi e b eeding ogs ha e no means o ejec unwan ed males. He e we desc ibe emale ma e a oidance beha iou s in he Eu opean common og. We obse ed h ee emale a oidance beha iou s, namely ‘ o a ion’,‘ elease call(s)’and onic immobili y (dea h eigning). These beha iou s we e signi ican ly associa ed wi h smalle emale body size, and smalle emales we e mo e success ul in escaping amplexus. Tonic immobili y as a ac ic o a oid ma ing o male ha assmen has only been obse ed in a hand ul o species and only in one o he amphibian. Ou obse a ions show ha emales in explosi e b eeding ogs may no be as passi e and helpless as p e iously hough . 1. Backg ound In classical sexual selec ion heo y, sexual selec ion is mos ly d i en by emale choice and male comba [1]. Acco ding o his heo y, bo h sexes aim o maximize hei ep oduc i e i ness. Whe eas males could ma e wi h se e al emales o inc ease he numbe o o sp ing, emales a e limi ed by hei ep oduc i e cycle and he numbe o po en ial o sp ing wi hin one o hose cycles, which is usually unchangeable [2]. Hence he cos s, bene i s and in e es s o bo h sexes may di e , which could lead © 2023 The Au ho s. Published by he Royal Socie y unde he e ms o he C ea i e Commons A ibu ion License h p://c ea i ecommons.o g/licenses/by/4.0/, which pe mi s un es ic ed use, p o ided he o iginal au ho and sou ce a e c edi ed. Downloaded om h ps:// oyalsocie ypublishing.o g/ on 23 Oc obe 2023 o sexual con lic [3] and sexual coe cion [4]. The mos d ama ic examples o sexual con lic a e in an icide, i.e. he so-called ‘B uce e ec ’, whe e he dea h o o sp ing s imula es o ula ion in he mo he s o some mammalian species [5,6], o he o ced copula ion beha iou o male wa e owl, which leads o an a ms ace educing he isk o o ced copula ion and unwan ed e iliza ion [7]. Thus, sexual con lic di ec ly gene a es selec i e p essu es and a ec s e olu iona y p ocesses [8]. Inc eased e o s by males (ha assmen , o ced copula ion, in imida ion) o gain access o emales could lead o ep oduc i e ailu e o indi iduals in ol ed and e en nega i ely a ec emale su i al (ducks: [9], ogs and oads: [10], mammals: [11]). In ogs and oads, a highe isk o mo ali y in ma ing emales has been epo ed, pa icula ly in explosi e b eeding species. This b eeding sys em is cha ac e ized by an (o en) male-biased ope a ional sex a io, synch onized emale ecep i i y and low sexual selec ion [12]. In explosi e b eeding anu an species, pai o ma ion is mainly d i en by male sc amble compe i ion o emales. Females could ei he be a ac ed by male ad e isemen calls o emain passi e, depending on he densi y a he b eeding si e [13]. Being ac i e as a emale includes he isk o being amplec ed by se e al males [13], which could lead o dea h o he espec i e emale [10,14,15]. The Eu opean common og, Rana empo a ia Linnaeus, 1758, is an explosi e b eede , o ming dense b eeding agg ega ions in ea ly sp ing [16]. Recen li e a u e, including comp ehensi e e iews, s a es ha emales a e passi e du ing cou ship and ep oduc i e beha iou [16], which is a ibu ed o sexual coe cion, pa icula ly emale ha assmen , by males. Howe e , he e is published e idence ha R. empo a ia emales a e no passi e du ing ep oduc ion. Mo e han 250 yea s ago, Rosenho [17] epo ed ha emales p oduce g un ing sounds like male elease calls [18]. This beha iou was obse ed a e emales ha e deposi ed eggs, hus signalling non- ecep i i y o a male [19]. In addi ion o hese calls, Sa age [19] obse ed emales showing onic immobili y (we he ein use his neu al e m ins ead o he mo e an h opocen ic ‘dea h eigning’) [20], when g abbed by a male, some imes o se e al hou s. Female common ogs a e he e o e unlikely o be de enceless agains sexual coe cion by males. He e we desc ibe emale ma e a oidance beha iou s obse ed du ing a ecen s udy o male ma e choice [21]. Ou obse a ions sugges ha emale common ogs a e no as passi e as is usually assumed, and ha age and expe ience may play a key ole in he pe o mance o hese beha iou s. 2. Me hods In sp ing 2019, we collec ed male and emale common ogs (Rana empo a ia) o es whe he males show a p e e ence o emale body size [21]. We placed wo di e en ly sized emales oge he wi h a male in a wa e - illed box (40 × 60 × 40 cm, 5 cm o wa e ) and allowed hem o mo e eely o one hou . We eco ded he ma ing beha iou in each box using a webcam (LogiTech 920). Female a oidance o male ma ing a emp s was obse ed by e iewing he ideo oo age. Fo de ails on loca ion and handling see Di ich e al. [21]. All aw da a and sc ip s o ep oducing he analysis a e s o ed in an online eposi o y [22]. We coun ed he occu ence o beha iou s alone, and in all possible combina ions (e.g. calls wi h o a ion and/o onic immobili y, e c.). We used a pai wise - es wi h p-adjus men o mul iple es ing ( alse disco e y a e) [23] o de e mine whe he emale body size di e ed when pe o ming speci ic beha iou s. We es ed his o he mos common ypes o beha iou s (sample size g ea e han i e). We modelled escape p obabili ies using a binomial logi model o emale body size pe se and he body size a io be ween emales and males. A body size a io abo e one means ha he emale is la ge han he male, and ice e sa i below one. We used he R s a is ical en i onmen [24] o all analyses and g aphs. We used he packages ggplo 2 [25], g idEx a [26], png [27] and ggsigni [28] o plo g aphs, MuMIn [29] o calcula e he likelihood- a io adjus ed R 2 o he binomial models and ply o coun he numbe o occu ences [30]. 3. Resul s We obse ed h ee emale a oidance beha iou s, namely ‘ o a ing’,‘ elease call(s)’and onic immobili y. We de ined ‘ o a ing’as a emale s a ing o o a e a ound he own body axis when amplexed by a male, while he male ies coun e ac ing he o a ion wi h i s hind ee (elec onic supplemen a y ma e ial, ideo S1). Release calls a e emi ed when he emale is amplexed by he male and she begins o call. Two di e en calls a e p oduced, a g un and a squeak (elec onic supplemen a y ma e ial, audio S2 and S3, see de ails in [18]). Tonic immobili y is de ined as he s i ening o he emale—a ms and legs oyalsocie ypublishing.o g/jou nal/ sos R. Soc. Open Sci. 10: 230742 2 Downloaded om h ps:// oyalsocie ypublishing.o g/ on 23 Oc obe 2023 ou s e ched om he body—a e being amplexed by a male (elec onic supplemen a y ma e ial, ideo S4). All h ee beha iou s we e obse ed when he ogs we e in wa e , bu we also obse ed one ins ance o onic immobili y in he e es ial habi a , be ween an 83 mm male and a 79 mm sized emale (elec onic supplemen a y ma e ial, igu e S5). In ou expe imen s, a o al o 54 emales we e amplexed by a male. The mos common emale ma e a oidance beha iou was o a ing, which was exhibi ed by 83% o all amplexed emales, ei he alone o in combina ion wi h he o he wo beha iou s. We also obse ed emale body o a ion in he na u al habi a se e al imes, sugges ing ha i is a common beha iou . Release calls we e emi ed by 48% o amplexed emales, and calls we e always associa ed wi h o a ing ( igu e 1a). Tonic immobili y occu ed in 33% o all clasped emales, mos o en in combina ion wi h o a ing and calling (13/18). The occu ence o all h ee beha iou s oge he was signi ican ly associa ed wi h smalle emale body size, whe eas o a ing in combina ion wi h calling was associa ed wi h la ge emale body size (pai wise - es wi h d co ec ion, p= 0.02, igu e 1b). Displaying o ma e a oidance beha iou esul ed in he escape o 25 emales (46% o all emales in amplexus). The p obabili y o escape showed a end o inc ease wi h dec easing emale body size (binomial GLM; p= 0.06, igu e 2a), and wi h dec easing emale- o-male SVL a io (smalle emales, binomial GLM; p= 0.09, igu e 2b). 4. Discussion Eu opean common og emales displayed body o a ions, elease calls and onic immobili y in o de o escape amplec ing males. Small emales used all h ee ma e a oidance beha iou s mo e equen ly han la ge emales and had highe escape p obabili ies. While se e al ma e a oidance beha iou s we e exhibi ed by emales, body o a ion was he mos common beha iou when a emale was clasped by a male. In o de o main ain an up igh posi ion and o keep holding he emale, males coun e ac ed he o a ion by using hei s e ched hind ee . This beha iou has been desc ibed by Sa age [19] bu was ne e subsequen ly epo ed o ci ed. The e could be se e al easons o he e ec i eness and high equency o emale o a ion. Ro a ing he male unde he emale and he eby unde wa e migh o ce males o elease emales o a oid d owning and enables emales o b ea he. Female o a ions could also be a s a egy es ing he s eng h and endu ance o males. Ma ing wi h a s onge male could inc ease a emale’s su i al p obabili ies. I a male can kick-o i als and hus p e en he o ma ion o a ‘ma ing ball’, he emale is mo e likely o su i e he ep oduc i e season [10,14,15]. Females may he e o e es po en ial ma es. Howe e , es ing po en ial ma es can also be cos ly [31], pa icula ly i a emale ecei es mo e a en ion h ough his beha iou bu canno de end he sel agains sexual coe cion om mul iple 15 10 5 0 o a ing o a ing onic immobili y o a ing + calling o a ing + calling o a ing + onic immobili y o a ing + calling + onic immobili y o a ing + calling + onic immobili y emale a oidance beha iou SVL emales (mm) none 55 60 65 70 75 80 85 90 app oached emales showing a oidance beha iou a oidance beha iou s (a)(b) Figu e 1. (a) Coun da a o all di e en a oidance beha iou s in common og emales, (b) emale body size in mm and a oidance beha iou displayed. Females displaying all h ee beha iou s we e on a e age signi ican ly smalle han emales displaying o a ing and calling (pai wise - es wi h d co ec ion, p= 0.02). La ge whi e do s ep esen mean body size, whiske s he 95% con idence in e al. Do s a e ji e ed o be e isibili y. oyalsocie ypublishing.o g/jou nal/ sos R. Soc. Open Sci. 10: 230742 3 Downloaded om h ps:// oyalsocie ypublishing.o g/ on 23 Oc obe 2023 males. I emains o be de e mined which (pheno ypic o geno ypic) ai (s) is (a e) unde selec ion, leading o ma e accep ance o ejec ion, and wha bene i s and cos s, i any, a e associa ed wi h ma e choice by emale R. empo a ia. The e seem o be no ob ious di ec bene i s o choosing a pa icula male, as males p o ide no pa en al ca e o de end any esou ces. Di ec bene i s, such as inc eased e iliza ion success by la ge o size-asso ed males ha e been disp o ed; in ac , e iliza ion success has been ound o be independen o size asso men [32]. We also de ec ed a high a e o mul iple pa e ni y in ou s udy popula ion (80% [33]), p obably due o ‘s ay spe m’, which would minimize he po en ial adap i e e ec s o p ecopula o y emale ma e choice. In e es ingly, smalle emale common ogs we e mo e success ul a escaping an amplexus by o a ing han la ge emales. This may be due o mechanical g ip cha ac e is ics. I emales a e (much) smalle han he amplexing male, he male may no be able o hold hem igh enough o main ain he amplexus. In Cane oads (Rhinella ma ina) i has been shown ha males wi h sho e a ms a e be e a holding on o emales han males wi h longe a ms. The la e a e mo e o en eplaced by o he males because hey canno hold he emales p ope ly [34]. Likewise in he Common oad (Bu o bu o), male akeo e s we e mo e success ul when pai s we e no size asso ed, i.e. size misma ch led o weake bonding in amplexus [35]. In ou s udy popula ion, we ound size-asso a i e ma ing [21,32], whe e he males a e usually smalle han he emales. A highe escape p obabili y o smalle emales amplexed by la ge males could be due o mechanical g ip p ope ies o he pai and suppo s he p e iously documen ed size-asso a i e pa e ns in he absence o male ma e choice [21,32]. Tonic immobili y is known o occu h oughou he animal kingdom, anging om in e eb a es o e eb a es [20]. I is mainly in e p e ed as a de ensi e s a egy agains p eda ion [36]. As a s ess esponse o an immedia e h ea o p eda ion (o a s ong ac ile s imulus), i is an ‘e olu iona y conse ed de ensi e mechanism o las eso ’[37]. Tonic immobili y as a ac ic o a oid ma ing, ep oduc i e cannibalism o male ha assmen , has been obse ed in a hand ul o species, mainly in a h opods such as spide s [38] and d agon lies [39], and in one o he amphibian species, he sha p- ibbed new (Pleu odeles wal l; [40]). Sa age [41] epo ed a emale R. empo a ia ha showed onic immobili y ( eigned dea h) o wo hou s a e being amplexed by a male. The male called equen ly du ing his ime bu did no le he go. We ha e obse ed onic immobili y by emales equen ly, bu mo e o en in smalle and he e o e younge emales. The smalle emales also showed he ull epe oi e o beha iou s mo e o en han he la ge emales. We he e o e specula e ha his beha iou may be ela ed o age o expe ience o emales. S ess inc eases co icos e one ci cula ing in he blood, which could inhibi ep oduc i e beha iou [42] and is posi i ely co ela ed wi h he du a ion o onic immobili y [37]. Less expe ience wi h ep oduc ion may esul in mo e s essed emales [20,43,44]. In he Ame ican wood og (Li hoba es syl a icus), a species which is e y simila in mo phology and beha iou o he Eu opean common og, emales showed a highe s ess esponse 1.00 1.00 0.75 0.50 0.25 0 0.75 0.50 0.25 0 escape p obabili y 60 70 SVL emale (mm) SVL a io ( emale/male) 80 90 0.8 1.0 1.2 1.4 (a)(b) Figu e 2. (a) Escape p obabili y o emale common ogs du ing a oidance beha iou as a unc ion o emale body size (SVL), o (b) he emale- o-male SVL a io. Do s ep esen indi idual emales and hei espec i e a oidance beha iou , ligh o ange = o a ing, o ange = o a ing and calling, ed = o a ing, calling and onic immobili y. Do s a e ji e ed o be e isibili y. oyalsocie ypublishing.o g/jou nal/ sos R. Soc. Open Sci. 10: 230742 4 Downloaded om h ps:// oyalsocie ypublishing.o g/ on 23 Oc obe 2023 du ing b eeding when male sc amble compe i ion was high [45]. An impo an sou ce o s ess, ha could igge onic immobili y, is he equen ly obse ed o ma ion o ‘ma ing balls’, which o en esul in he dea h o emales and males by d owning [10,14,15]. Whe he d owning (lack o oxygen) is he main ac o leading o dea h is no en i ely clea , especially as his species is able o abso b oxygen om he wa e h ough he skin and pa ly hibe na es in ponds o s eams [41]. I may be a mix u e o ac o s ha lead o he dea h o indi iduals du ing hese ma ing balls. Tonic immobili y can lead o b adyca dia and he e o e an inc ease in pe iphe al esis ance [37], which could educe oxygen up ake h ough he skin. Du ing he igh , wa e may en e he lungs, u he educing oxygen up ake. B eeding begins immedia ely a e hibe na ion and indi iduals do no eed be o e joining he b eeding g oup [46], esul ing in high ene gy demands ha may no be me , leading o allos a ic o e load and dea h [47]. Ano he ac o could be he high p essu e exe ed by he amplexed males, which could damage he emale’s o gans and lead o egg ex usion [10]. Anyhow, wha he p oxima e ac o killing he emales may be, onic immobili y may be a be e op ion o a emale han igh ing he way ou o he amplexus, as any mo emen in a la ge ma ing g oup au oma ically a ac s a en ion o u he nea by males and hus inc eases he p obabili y o a ma ing ball o ma ion. Wi h hese conside a ions in mind, i would be in e es ing o measu e s ess co icos e one le els in emale R. empo a ia and in es iga e how hey co espond o age and sex a io in b eeding agg ega ions [45,48]. Fu u e s udies should conside in es iga ing di e en og densi ies, sex a ios and age classes, o es o ma e choice and he po en ial cos s associa ed wi h ep oduc ion. Howe e , ou s udy p o ides clea e idence ha emale ogs, e en in dense ma ing agg ega ions o explosi e b eede s, a e less helpless han gene ally assumed. E hics. The go e nmen om Lowe F anconia issued esea ch pe mi s (55.2 DMS 2532-2-316) and he Ba a ian s a e o es y depa men pe mission o access he o es ponds. All animal beha iou al expe imen s ollowed he guidelines p o ided by ASAB. Da a accessibili y. The aw da a a e deposi ed oge he wi h a eadme ex ile o me ada a, desc ip ion o a iables and he R-sc ip o ep oduce all analysis and igu es. The DOI is p o ided in he e e ences [22]. h ps://doi.o g/10.7479/ s00 - a45. The audio and ideo iles a e p o ided in elec onic supplemen a y ma e ial [49]. Decla a ion o AI use. We ha e no used AI-assis ed echnologies in c ea ing his a icle. Au ho s’con ibu ions. C.D.: concep ualiza ion, da a cu a ion, o mal analysis, unding acquisi ion, in es iga ion, me hodology, p ojec adminis a ion, w i ing—o iginal d a , w i ing— e iew and edi ing; M.R.: concep ualiza ion, unding acquisi ion, in es iga ion, me hodology, esou ces, supe ision, w i ing— e iew and edi ing. All au ho s ga e inal app o al o publica ion and ag eed o be held accoun able o he wo k pe o med he ein. Con lic o in e es decla a ion. We decla e ha ing no compe ing in e es s. Funding. This s udy was suppo ed by a PhD schola ship om he s a e o Be lin (Elsa Neumann Founda ion) awa ded o CD. Ma e ial cos s we e co e ed by he Museum ü Na u kunde Be lin. Acknowledgemen s. We hank he ollowing people o hei suppo du ing ieldwo k and sigh ing o ideo ma e ial. Melanie Tie je, Ya a Ha idy, Guillaume Dema e and Ju ek Ri z. We hank he s a o he ecological ield s a ion, Uni e si y o Wü zbu g, p o iding access o c ucial in as uc u e. We a e indeb ed o he go e nmen om Lowe F anconia o esea ch pe mi s and he Ba a ian s a e o es y depa men o access pe mission o he o es ponds. The og icon used in he igu es is p o ided by la icon.com unde he Fla icon licence. Thanks o he au ho Vic o ule o he c ea ion. We hank he edi o and wo anonymous e iewe s o hei aluable commen s. Re e ences 1. 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