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Article: Ball, A.D., van Dijk, R.E., Lloyd, P. et al. (6 more authors) (2017) Levels of extra-pair paternity are associated with parental care in penduline tits (Remizidae). Ibis, 159 (2). pp. 449-455. ISSN 1474-919X https://doi.org/10.1111/ibi.12446

This is the peer reviewed version of the following article: Ball, A. D. et al (2016), Levels of extra-pair paternity are associated with parental care in penduline tits (Remizidae). Ibis, which has been published in final form at http://dx.doi.org/10.1111/ibi.12446. This article may be used for non-commercial purposes in accordance with Wiley Terms and Conditions for Self-Archiving.

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[email protected] https://eprints.whiterose.ac.uk/ This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. 10.1111/ibi.12446doi: lead todifferences version between this cite Please of andthe article Record. Version this as been and typesetting, through which may proofreading thecopyediting, process, pagination This article undergone has for buthas and accepted been not review publication full peer Runninghead: Extra-pair paternity in penduline tits Reynolds Jim Editor: Article type Communication :Short Accepted Date :03-Dec-2016 Received :17-Feb-2015 Date 1 6

4 Levels of extra-pair paternity are associated with parental parental with associated are paternity of extra-pair Levels 2 3 Department Biology of and Biochemistry, UniversityBath, of Department Biology, of Syracuse University, College Plac 107 5

AcceptedBiodiversity Assessment and Management Ltd, Pty PO Box 1376, Article

Department Percy FitzPatrick Institute Africanof Ornithology,Universit Department Ethology, of Loránd Eötvös University,Pázmány DAWSON, ALEX BALL,D. 2 of STEVE DORUS,

Animal and Plant Sciences, University of Sheffield, West 1,2, care in penduline tits (Remizidae) (Remizidae) tits inpenduline care * RENÉ *E. RENÉ DIJK, VAN 1,6 RAURI K.C. BOWIE, Cape SouthTown, Africa 1 ,2 Hungary 2TN, UK 2TN, PENN LLOYD, USA

3, 7 TERRY BURKE 3 ,4 ÁKOS POGÁNY, y Capeof Town, Rondebosch 7701, Claverton Down, Bath, BA2 7AY, UK e, Syracuse, York, New 13244-1220, Péter Budapest, 1/C, S. 1117, H- Cleveland, Qld Australia4163, 2 & TAMÁS SZÉKELY er n Bank, Sheffield, S10 5 DEBORAH A. 1

oee, nesadn te ramifications the understanding However, rmmlil mtns (Kempenaers matings multiple from fo therefore has Research 2000). Nilsson & Arnqvist 1 (Parker females by matings multiple of prevalence Kokko 2006, Cockburn 1992, Parker & (Clutton-Brock th to exception an as seen often are However, mates additional seek to likely more are males that (Bateman 1948; Clutton-Brock & Vincent 1991; Kokko Kokko 1991; Vincent & Clutton-Brock 1948; (Bateman females whereas mates of number their increasing by 2008) Jennions & Kokko 1994, Bennett & Owens 1972, future of expense the at fitness offspring enhance to predicted are systems mating and care Parental todue the devaluing paternal of care by extra-pair (Remizidae) tit p extra-pair of incidence the and care male between a parentage and observations nest use We sexes. the fitness the since occur to predicted is behaviours ae hl as mtn otie hi pi bond pair their outside mating also while care This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. In Email: [email protected] *Corresponding author. 7 ot asrn brs idvdas tep t maxim to attempt individuals birds, most

Accepted Article Museum of Vertebrate Zoology Department& Integrative of Bio Building, University . This provides evidence of a trade-off between these between trade-off a of evidence provides This of California, Berkeley,California 94720-3160, USA et al. et 1992, Jennions & Petrie 2000, Griffith 2000, Petrie & Jennions 1992, of of hs promiscuity this . offspring. reproductive success (Williams 1966, Trivers 1966, (Williams success reproductive benefits of extra-pair mating differs between differs mating extra-pair of benefits sxseii taeof ewe tee two these between trade-off sex-specific A whilst females provide care (Trivers 1972) (Trivers care provide females whilst co cussed on the benefits females might gain might females benefits the on cussed aternity across three species of penduline of species three across aternity 970, Birkhead & Møller 1992, Yasui 1998, Yasui 1992, Møller & Birkhead 970, -evolve because parental care is likely to likely is care parental because -evolve ayi t rva a eaie association negative a reveal to nalysis s ue s ot xii bprna care biparental exhibit most as rule is . et al. et s ter ins b poiig parental providing by fitness their ise Males are predicted to enhance fitness enhance to predicted are Males r cntand y hi fecundity their by constrained are & Jennions 2008) and have a high high a have and 2008) Jennions & , 2006) , logy, 3101logy, Valley Life Sciences for . aetl ae investment care parental Theory therefore predicts therefore Theory two behaviours, two et al. et po

2002) ssibly . . This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. necessar is 2002) Sheldon 1992, Sherman & (Westneat oeta ifune n h ftes eeis associa benefits fitness the on influence potential syste care parental and mating between relationship evolutionary relationships betweentraits these (Ko soitd ih hi ptra cr; a care; paternal their with associated tur in and, paternity multiple with broods produces ai (ok & Jennions & (Kokko ratio care female, not but male, in decrease a for select 199(Queller care maternal to apply not does (EPCs) example example ex acros promiscuity female and male and care parental pendulinus strategies, parental diverse exhibit tits penduline fo attention garnered has that group a on focussing of levels confirmed higher with species in care male reduced potentially at the expenseprovidi of populations and repeatable within individuals (Pers individuals within repeatable and populations 2010 van Dijk males are less likely to provide care than females females than care provide to likely less are males The Eurasian exhibits high levels of levels high Dijk exhibits Tit PendulineEurasian The (van care parental male of

Acceptedists Article a . , hr sc a oprtv apoc hs en pursued, been has approach comparative a such Where e suis ae netgtd h eouinr dyna evolutionary the investigated have studies Few Two factors beenTwo have identifiedthat arelikely to Pogány et al. a (M eaebae sx ai poie icesd opportun increased provides ratio sex female-biased xiiig nsa sxseii pten o cr, w care, of patterns sex-specific unusual exhibiting

øller & Birkhead 1993, Arnold & Owens 2002). We aim We 2002). Owens & Arnold 1993, Birkhead & øller 2010 t al. et a) .

08. rvos ok a fcse o dtriig t determining on focussed has work Previous 2008). 2008) wih s cnrl atr nlecn mt acquis mate influencing factor central a is which , et al. et ng paternal care.

n 2010 qiaet eauto de o xr-ar copulation extra-pair to due devaluation equivalent b) . ae s las nprna i ti seis and species this in uniparental always is Care (Szentirmai kko & Jennions 2008). . The second variable is the population sex population the is variable second The . e wt ptra cr. Female care. paternal with ted 7). Thus, in most species, polyandry shouldpolyandry species, most in Thus, 7). with the Tit Penduline Eurasian the with r its unusual parental care behaviour. The behaviour. care parental unusual its r son & Öhrström 1989, 1989, Öhrström & son ms. The first is female promiscuity and its and promiscuity female is first The ms. , eue te ins bnft t males to benefits fitness the reduces n, seis es hr sial variation suitable where sets species s xr-ar aent (P) a been has (EPP) paternity extra-pair have implications have evolutionaryforthe EPP (24% of offspring) and low levelslow and offspring) of (24% EPP i w ae o nesad the understand to are we if y iso te eainhp between relationship the of mics et al. et h peitd eainhp of relationship predicted the ih r cnitn across consistent are hich te fr ae t re-mate, to males for ities

2007 to further this work by work this further to , van Dijk van , Po gány e atr that factors he et al. et et al. et re ition; for for ition; -mating

2007, 2007, 2008 co s - , This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. beh desertion sex-biased widespread, this influence 2005 suggesting that parental behaviour parental that suggesting populations European across consistent is strategy 2008 Tit c two on data new with it combine and Tit Penduline The was studied over a six-year six-year a over studied was Tit Penduline Cape The METHODS associatedare with reducedpaternal care. t to EPP characterise to analyses genetic molecular was studied in 2008 in the Tien Shan foothills near foothills Shan Tien the in 2008 in studied was studied from 2002 we which from population Tit Penduline Eurasian The Reserve, Western Cape, (33° (33° Africa South WesternCape, Reserve, provide a detailed description of parental care sys care parental of description detailed a provide between relationship co-evolutionary the understand idvriy f aahtn Bod samples Blood Kazakhstan. of Biodiversity th of stewardship the under conducted and committee All adult birds were ringed with a numbered metal numbered a with ringed were birds adult All plasticthree colour rings ( The White-crowned Penduline Tit work was approved b approved was work Tit Penduline White-crowned The W the underandconductedby issuedpermits SAFRING C Ethics the by approved were Tits Penduline stored in 1 1 in stored Accepted Article

nhsou minutus , van Dijk Dijk van , , van Dijk Dijk van ,

ml of Queens of ml et al. t al. et 20

2008 08, 2010a) 2008a, 07 07 atFehé n te ht-rwe Pnuie Tit Penduline White-crowned the and a, 2012, Pogány 2012, a, Lysis Buffer (Seutin Buffer Lysis XF A.size, Hughes,C. London, UK). rt ó ó fishpond system is .

un hs w da o eitn kolde f h Eurasian the of knowledge existing on draw we Thus, responsive to local environmental cues (Pogány cues environmental local to responsive et al. S, 18° S, (~ et al.

2012 10

est the prediction that greater levels of EPP of levels greater that prediction the est tems ) ee ae fo te rcil en and vein brachial the from taken were l) Jabagly, Kazakhstan (42° (42° Kazakhstan Jabagly, 1991) , , despite variation in mating opportunities, mating in variation despite Hungary (46° losely-related species, the Cape Penduline Cape the species, losely-related vor (Valer aviour 201 ommittee, University of Cape Town, and Town, Cape of University ommittee, E) and the White-crowned PendulineWhite-crownedtheTit and E) eid (2002 period estern Cape Nature ConservationNature esternCape Board. rmsut ad aetl ae We care. parental and promiscuity , Ascain o te osrain of Conservation the for Association e y the University of Bath of University the y calculate offspring sex ratios and use and ratios sex offspring calculate 5) . eeae xsig nomto was information existing leverage Across all years the total number of number total the years all Across . Importantly, this unusual parentalunusual this Importantly, ring and a unique combination of combination unique a and ring Th e e capture and samplingCape of a N ei coronatus Remiz et al. et 07 a Keeg Nature Koeberg at 2007)

1997 ° 0 ° E Bleeker , N, 70° 70° N, Ani

o better to mal Ethics mal et al. et et al. et

E) .

edln Tt 1 nss Ersa Pnuie i: 13 Tit: Penduline Eurasian nests, 18 Tit: Penduline ma observations through recorded was care Parental (C birds adult of behaviour and identity the noting 1 This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. T Penduline Cape the in 194 was birds blood-sampled (12 videos from calculated also were rates provisioning mea a as recorded was nest the in spent parent each blood samples were genotyped (211 adults and 443of obtained from 63 birds (32 and adults nestlings)31 years) subsequent in allocat likeli the assesses which 2.0.5), (v COLONY program (Table populations microsatellitemar 17 using assigned was Parentage Tit Penduline White-crowned and nest. allowed footage, video by supported care, nestling colour-r of observations continual our Thus, nest). crowned Penduline Tit nests ( nests Tit Penduline crowned at recorded assigned correctly if they had a likelihood score likelihood a had they if correctly assigned assignm conservative the to Due 2010). Wang & Jones behaviour during the latter stages of incubation (8 incubation of stages latter the during behaviour 2014 Accepted Article 35 nestlings 5 as oththn) t ie ae edln Tt n Tit Penduline Cape five at post-hatching) days 15 ). es aent ad aent va mxmm ieiod m likelihood maximum a via maternity and paternity six , plus an additional eight birds that wereassampled that birds additionalan plus eight Cape Penduline Tit nests ( nests Tit Penduline Cape . o te ht-rwe Pnuie i pplto, blo population, Tit Penduline White-crowned the For 173 ±7 minutes of footage per nest) per footage of minutes ±7 299 ± 44 minutes of footage per nest) and nine White- nine and nest) per footage of minutes 80 ape Penduline Tit: 21 nests, White-crowned nests, 21 Tit: Penduline ape and in the Eurasian and inPenduline Eurasian the Tit 654study us to identify the care provider(s) at each at provider(s) care the identify to us hood of sibships within the population and population the within sibships of hood taken in the latter stages of nestling care nestling of stages latter the in taken % (as in Bergner in (as % nests) 8 12 days after the last egg was laid) were laid) was egg last the after days 12 fspring; van Dijk ne brs hogot nuain and incubation throughout birds inged it population ( population it ue f nuain netet Parental investment. incubation of sure ent of COLONY, birds were accepted as accepted were birds COLONY, of ent ) Ptriy a alctd sn the using allocated was Paternity 1). ss 373 mnts f otg per footage of minutes (317±38 ests kers for both the Cape PendulineTitCape the both for kers . e vr to as t ah nest each at days two every de diinly vdo o parental of videos Additionally, to (ag Snue 2009, Santure & (Wang ethod nestlingsandadults recruited . The percentage of time that time of percentage The 38 et al. et al. adults, 13 juveniles andjuveniles 13 adults,

2010b 2014 d ape were samples od , Gamero , ).

et al. ,

This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. desert c paternal whether test to used was structure error oe t alvae h polm o cmlt separat complete of problems the alleviate to model ne multiple male same the because term random a as included was C or Tit PendulineWhite-crowned (Eurasian, species offs of percentage (the nest a in EPP of amount the did not differ from parity in either Cape Penduline Cape either in parity from differ not did the parentage analyses are provided in Table 1. The 1. Table in provided are analyses parentage the Detai females). 13 males: 19 Tit: Penduline crowned ubr f dl mls n fmls Cp Pnuie T Penduline (Cape females and males adult of number were Tits Penduline White-crowned nestlings) 31 and Accepted1 of total A Microsatellite genotyping and sex-typing RESULTS laboratory methodology can beSupplementar found in Tit Penduline Cape and Tit Penduline White-crowned expect the from deviations any for test to used was (v nestlings of rate provisioning the or incubating effec the for test to test ratio likelihood a using Article(witho model null the and models all in term random Tit Penduline Cape and Tit Penduline White-crowned li a using tested were rates feeding and incubation ) was explained by EPP in our model. The explanator The model. our in EPP by explained was ) A Bayesian generalized linear mixed mode mixed linear generalized Bayesian A

67 sting attempts A normal A attempts sting ( 34 adults, 13 juveniles and 120 nestlings) Cape Pendu Cape nestlings) 120 and juveniles 13 adults, -prior was applied to the fixed effects when runnin when effects fixed the to applied was -prior t of sex on either the proportion of time spent time of proportion the either on sex of t Tit offspring (62 males: 58 females, binomialfemales, 58 males: (62 offspring Tit ed equal sex ratio in the entire population ofpopulation entire the in ratio sex equal ed isits/hour). A two-sided binomial exact test exact binomial two-sided A isits/hour). l BGLMM R Package blme Package R BGLMM l overall sex ratio of 9 of ratio sex overall ape Penduline Tit) as fixed effects. Male ID Male effects. fixed as Tit) Penduline ape er ie mdl prah o bt the both for approach model mixed near ut sex) and the full model were compared were model full the and sex) ut ls of the microsatellite loci genotyped for genotyped loci microsatellite the of ls rn urltd o h sca fte) and father) social the to unrelated pring y OnlineAppendix S1. r (iay response (Binary are nestlings. Additional details of field and field of details Additional nestlings. genotyped, including a roughly similar roughly a including genotyped, o i te dataset. the in ion eaaey Ns I ws nldd s a as included was ID Nest separately. it : : a ocsoal osre across observed occasionally was 6 ae: 8 females 18 males: 16 y variables of the model included model the of variables y line Tits and 63 (32 adults(32 63 and Tits line

10 day old nestlings old day 10 e dfeecs in differences Sex aibe ae or care variable ) with binomial with ) , n White- and g the g This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. test exact females, binomial exact test,two-tailed; n h Cp Pnuie i, aetl ae a provid was care parental Tit, Penduline Cape the In Patterns of parental care the male (t male the nests 14 at provisioning nestling through continued female and male the both population, Tit Penduline the Of pair. the of nest previous a from juvenile a observed provisioning the nest in addition to the f observed nests until fledging of offspring offspring of fledging until nests observed Dijk Dijk exhib nests remaining the with 79%) nests; (109/138 nestli Tit Penduline the Eurasian the in in Contrastingly, roles care sex-specific for evidence no with Of the the Of Parentage analysis provisioning (Figure 1) (Figure provisioning contained extra-pair young (15.4% (15.4% youngextra-pair contained a single a single social parent was genotyped havinnestlings(7.1%)42 of outthree in resulting nests, a total total a nests, caring female. low This level consistent IBP is of Accepted para brood intraspecific of result the (1%) one and Article et al. 13 13 2010b) , Cape Penduline Tit nests where the social mother an mother social the where nests Tit Penduline Cape wo two-tailed; of of nests; 11%) or the female (t female the or 11%) nests; four nestlings). In these nests, three chicks of 97 of chicks three nests, these In nestlings). four .

. P

The video footage supported the field observations field the supported footage video The 0. = 78 ) or of of , ht-rwe Pnuie i ofpig 1 mls 1 males: (18 offspring Tit Penduline White-crowned three theof three 28 contained nests extra-pair young (1 nests). These three extra-pair young were caused by caused were young extra-pair three These nests). P = wo (n 0.47 2) A sx 2% o tee et a epr was helper a nests these of (29%) six At 21). = nests; 11%) ceased parental care before nestling before care parental ceased 11%) nests; ) using the with observedlow the rates theacross majority ocal pair andidentified thisocal in one was case pair as g EPP (Figure 2). When includingwherenestsWhen 2). (FigureEPP g g ae s oiae b fml-ny care female-only by dominated is care ng 8 et osre i te White-crowned the in observed nests 18 carried out incubation, and biparental care biparental and incubation, out carried (78%). At the remaining four nests either nests four remaining the At (78%). iim IP ie oe a urltd o the to unrelated was one i.e. (IBP) sitism iting male-only care (29/138; 21%) (van 21%) (29/138; care male-only iting ed by both males and females females and males both by ed w suid pce (pedx S2). (Appendix species studied two Z-002A (3.1%) were the result of EPP of result the were (3.1%) ahrwr genotyped were father d sexing marker. of biparental care biparental of

0.7% of0.7% at , EPP, the two 3 negatively correlated with EPP (Møller & Birkh & (Møller EPP with correlated negatively le the that demonstrated that studyprevious a with rvdd y ot c 8% pseie pce (Cockbu species passerine 84%) (c. most by provided This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. IBP) from result offspring in including 2002) Owens & (Arnold species of parents with with parents nes all found; was offspring extra-pair of evidence 0 was offspring unrelated for caring be will female w brood per male social the to unrelated are 2). 2). disentangle the drivers of this relationship. stra care parental atypical and diverse with family Acceptedlower exhibit care female to compared male of rates sp closely-related three across evidence provide We DISCUSSION collinearityof complicates interpretation. o 0% and 42 of (7.1% Tit PendulineWhite-crowned or EPP from (24% nestlings) 166 of than that observed Articlesub exhibits Tit Penduline Eurasian the as However, E the in prevalent more significantly was desertion explai variable important most The 2). (Table nests In our BGLMM our In

97% likelihood at the five nests at which both soc both which at nests five the at likelihood 97% , EPP was a weak negative predictor of paternal care care paternal of predictor negative weak a was EPP . In the Cape Penduline Tit, the average percentage average the Tit, Penduline Cape the In as 5.4% (across 28 nests). The probability that a that probability The nests). 28 (across 5.4% ead .9%. In the White-crowned Penduline Tit no Tit Penduline White-crowned the In .9%. tlings (n = 29) were assigned to both social both to assigned were 29) = (n tlings vel of male care during chick provisioningis chickduring care male of vel urasian Penduline Tit population (Table 2). (Table population Tit Penduline urasian tegies may provide future opportunities to opportunities future provide may tegies ecies of penduline tit that those with higherwith those that tit pendulineof ecies

ning paternal care was species, as paternal as species, was care paternal ning in in the mostly biparental Cape Penduline Tit 1993) rates of EPP of rates stantially higher levels of young resulting young of levels higher stantially f 29, respectively; Figure 2), the problemthe 2), Figurerespectively; 29, f n 2006) rn h Ersa Pnuie i (.% of (6.6% Tit Penduline Eurasian the . Considering that biparental care is care biparental that Considering , . ial parents were known (Fig. known were parents ial ihihig hs eut n a in result this highlighting These results are consistent are results These across penduline tit penduline across of of offspring that offspring observed (Liker observed ra sex between association an ratio, sex population fa that birds of taxon a in However, 2007). (Donald birds, passerine small especially and species, bird p the in also ratio sex offspring of parity showing This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. associated providingwith paternal care. might fledging after caused Tit Penduline Eurasian (Liker sex each of opportunities mating second the was ratio sex operational or adult The bet and within both system care parental and mating nrae smls f et (Griffith nests of samples increased EP because and 1991), (Lott inferences species-wide observa extrapolating because nests and populations sex adult unbiased with consistent be would species combine EPP of rates low the adults, amongst ratios Penduline CapeTitand Penduline Although Tit). we c i nestlings of ratios sex the in bias a of evidence across geographically distinct populations (van Dij (van populations distinct geographically across Eurasia the of population single the in system care Penduline Tit populations Tit Penduline C single our in observed care parental that support addition, we acknowledge the need for increased sam increased for need the acknowledgewe addition, exception) and parental care in multiple populations of the sa the of populations multiple in care parental and the in both research, this of nature intensive the example, if we were to sample five nests in the Eur the in nests five sample to were we if example, Accepted Article e cnweg ta ti suy ol bnft rm i from benefit would study this that acknowledge We . Nonetheless, our results highlight a key difference key a highlight results our Nonetheless, et al. et 2013). We therefore cannot rule out that bias that out rule cannot therefore We 2013). is typical of each species, we require definitive evi definitive require we species, each of typical et al. et et al. et

2002 2014). In line with our prediction, we found no found we prediction, our with line In 2014). ). However, we would argue that the parental parental the that argue would we However, ). n the two biparental species (White-crowned species biparental two the n field and lab, few studies have assessed EPP assessed have studies few lab, and field olygamous Eurasian Penduline Tit). In most In Tit). Penduline Eurasian olygamous k asian Penduline Tit population (29/55 nests (29/55 population Tit Penduline asian me species (see Brommer (see species me t s ifcl t etmt aut e ratios sex adult estimate to difficult is it n Penduline Tit is typical of that observed that of typical is Tit Penduline n annot rule out the possibility skewed of sex i ad aetl ae eaiu hs been has behaviour care parental and tio et al. d with biparental care found in these two these in found care biparental with d e epnil fr ifrn ftes costs fitness differing for responsible be iiae oe cuae siain o the of estimations accurate more cilitate ple sizes in EPP studies in general in studies EPP in sizes ple ween species, as it potentially skews the skews potentially it as species, ween p Pnuie i ad White-crowned and Tit Penduline ape etmts nrae n cuay with accuracy in increase estimates P ais bt e vn Dijk van see (but ratios in fo a ige ouain limits population single a from tions

2010 aibe rdce t ifune the influence to predicted variable worth further investigation. For investigation. further worth a). Although this provides some provides this Although a). ncreased sample sizes sizes sample ncreased ed adult sex ratios in the in ratios sex adult dence dence et al.

t al. et 2010 for this . for an for Due to Due 2008b . In of of This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. Eurasi the in EPP from resulting young contain that (18% Tit Penduline Cape the in EPP containing nests Penduli White-crowned the in case the was as young, likelihood the EPP) from resulting chicks contained Griffith mult a require the of likely one remains rates will promiscuity in it Diversity tackle to and biology to the evolution of parental behaviour. care related species, are likely to generate novel insig novel generate to likely are species, related ae bten populations between rates intraspecific variation in EPP in variation intraspecific differences in mating and parental care among popul among care parental and mating in differences Kazakhstan for logistic support. Thanks are also ex also are Thanks support. logistic for Kazakhstan White-crown Associat the at Sklyarenko Sergey the to and Kazakhstan on fieldwork the conducting support Sander to go thanks Our Reserve. Nature Koeberg at CapeNa and ESKOM Greef, Gert as well as population, wh assistants field many the thank to like would We that could explain diversity in breeding systems mo t system model informative an provide therefore may in observed care paternal reduced and EPP of levels and care biparental exhibit Tit Penduline Cape and level with associated are that family tit penduline assortme an confirmed has study Our traits. history 2

Accepted Article 1, = df 4.5, = t al. et 02 Kko Jnin 2008) Jennions & Kokko 2002, P = 0.03). Thus, even low sample sizes can reveal a reveal can sizes sample low even Thus, 0.03). = . However, we hope future research effort will focus focus will effort research future hope we However, , the underlying reasons for this variation and how t how and variation this for reasons underlying the . e ol age ae o or idns that findings our on based argue would We hts into the into hts s of EPP. The White-crowned Penduline Tit Tit Penduline White-crowned The EPP. of s re generally.re high levels of fidelity, in contrast to the high the to contrast in fidelity, of levels high fctd prah Anl & wn 2002, Owens & (Arnold approach ifaceted an Penduline Tit (Pearson chi-squared test, chi-squared (Pearson Tit Penduline an the Eurasian Penduline Tit. The Remizidae The Tit. Penduline Eurasian the tended to Douglas Ross, Jim Reynolds and Reynolds Jim Ross, Douglas to tended o collected data on the Cape Penduline Tit Penduline Cape the on data collected o ion for the Conservation of Biodiversity of Biodiversity of Conservation the for ion ture for permissions and permits to work to permits and permissions for ture ) is also significantly lower than the 53% the than lower significantly also is ) ations within species and among close among and species within ations f ann ol nss ih within-pair with nests only gaining of t f aetl ae ytm ars the across systems care parental of nt e i, s ny .% Te rprin of proportion The 3.4%. only is Tit, ne ts seii eouinr hypotheses evolutionary specific test o o ad ea oooa o hl and help for Voronova Vera and Bot most puzzling topics in evolutionary in topics puzzling most d edln Tt ouain in population Tit Penduline ed co -evolution of these critical life- critical these of -evolution significant difference significant his may relatemay his n assessing on in EPP ly - This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. Europea the from funding received has results these anonymousthree reviewers providingfor comments on Arnqvist, G., & Kirkpatrick, M. Arnold, K.E. & Owens, I.P.F. REFERENCES (NBAF361). (NERC) and performed at the NERC Biomolecular AnalyBiomolecular NERC the at performed and (NERC) REvD and ADB. molecular The work was funded by the Uni two from and REvD, to [SBP/JK/2007-53] Sciences Poppingfonds Schure-Beijerinck N the from Hungarian [K109337], the from PL, and AP, TS, to 00564/2006] Hungarian-South the from support financial further nu contract under FP6/2002-2006) (GEBACO; Programme Arnqvist, G. & Nilsson, T. Bateman, A.J. Bergner, L.M., Jamieson, I.G. & Robertson, B.C. Birkhead, T.R. & Moller, A.P. Bleeker, M., Kingma, S.A., Szentirmai, I., Székely, T AcceptedBrommer, J.E., Alho, J.S.,Biard, C., Chapman, J.R. Article parental care and the risk retaliation.of in in insects. females. : the strength of direct and indirect sel relatedness among founders in a genetically depaupe habroptilus clutch desertion Penduline in Tit, consequences Lubjuhn, T., Patrick, S.C., Rosivall, B., Tinbergen, Hjernquist, M.B., Kempenaers, B., Komdeur, J., Laakso Am. Nat. Intra-sexual1948. selection in Drosophila. Anim. Behav. ). Conserv. Genet. . Academic Press, London, UK.

165 The2000. evolution of polyandry: multiple mating a : : S26

60 Extra-pair2002. paternity and egg dumping in bird 1992. : 145

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15 : 1013 Sperm competition in Birds: Evolutionarycauses and 164. . The evolution infidelity of in socially monogamous Remiz pendulinus

1020. Proc. R. Soc. B Biol. Sci. Combining2014. genetic data to identify

, Charmantier,, A., Dreiss, A.,Hartley, I.R., . & Komdeur, J. ection on extrapair copulation behavior in fia Itroenetl É [OMFB- TÉT Intergovernmental African Natural Environmental Research Council versity of Bath studentships awarded to awarded studentships Bath of versity the manuscript. The research leading to . sis Facility sis f h Ryl ehrad Aaey of Academy Netherlands Royal the of Behaviour J.M., der van Velde, M., Oers, van K., Heredity. rate parrot, the Kakapo ( C n toa Sine onain OTKA Foundation Science ational br 89. h wr received work The 28696. mber nen, T.,nen, Lehtonen, P.K., ommunitys

2

at 142 269 : 349 Body2005. condition and the University of Sheffield of University the : 1465 : 1263 368. it Framework Sixth nd female fitness 1478. 1269. s: life history, Strigops

Clutton-Brock, T.H. & Parker, G.A. Donald, P.F. Dawson, D.A. Cockburn, A. Gamero, A., Székely, & T.Kappeler, P.M. Clutton-Brock, T.H. & Vincent, A.C.J. Dawson, D. A., Ball, A.D.,Spurgin, L.G., Martin-Galv Dawson, D. A., Horsburgh, G. J., Küpper, C., Stewart, Griffith, S.C., Owens, I.P.F. & Thuman, K.A. This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. Jennions, M.D. & Petrie, M. Jones, O.R. & Wang, J. Kempenaers, B., Verheyen, G.R., Broeck,Van den M., Kalinowski, S.T., Taper, M.L., & Marshall, T.C. Kokko, H.Jennions, & M.D. Kokko, H., Jennions, M.D. & Brooks, R. Accepted Article approach comparing four species. Sci. sexual sexual selection. no cooperative breeding inWhite-breasted Mesites ( rates ofrates males and females. demonstrated birds. for conserved microsatellite loci and develop primer se Sociobiol. Burke, T. Potter, J., Molina-Morales, M., Bicknell, A.W.J., Pr Thesis,PhD University of UK.Sheffield, population studies across a rangewide of species. Simeoni, M., Smith, G., Spurgin, L.G. & Burke, T. Hansson, B., Bacon, I., Bird, S., Á., Klein, Krupa, A in Wilk, T. & Winkel, W benefits. multilocus genotype data. Dhont, A.A. Ecol. CERVUS accommodates genotyping error increases succ males in theBlue Tit. Biol. terspecific variation and adaptive function.

273

21 16 Adult2007. sex ratios in wild bird populations. : 919 : : : 2006. Prevalence2006. different of modes of parental car 1375 Biol. Rev. 1099

2007

68 2013 1992. Extra-pair1992. paternity results from female pref : 73 948. . 1383. 1106. . High-utility conserved avian microsatellite marke Genomic analysis passerine of usingbirds conserved Q. 83.

2010. COLONY:2010. a program for parentage andsibship i

75 Rev. Biol.

: 21 Nature . 2010. Passerine 2010. extrapair mating dynamics: a bayes Why2000. femalesdo mate multiply? A review of th Parental2008. investment, sexual selection and se Mol. Ecol. Resour. 64. Mol. Ecol.Mol. Resour. Nature

67 357

1992. Potential1992. reproductive rates and the operatio : : 437 1991. Sexual selection and the potential reproduct : 494 Am. Nat.

351 Unifying2006. and Testing Models of Sexual Select 456. 2014. Delayed 2014. juvenile dispersal and monogamy, but : 58 2002. Extra pair paternity in birds: a review of 496.

10

176 2007

10 60. : 475 Mol. Ecol. : 551

: 178 ez, D., Stewart, I.R.K., Horsburgh, G.J., . Revising how the computer program I. R. K., Ball, A. D., K. Durrant, L.,

BMC Genomics 2010 494. Burke, T., Van Broeckhoven, C. & .P., Lee, J., Martín-Gálvez, D., eston, S.A.J. Ekblom,Slate, J.R., & ts of high of ts cross-species utilityas- Mesitornis variegata 555. 187.

11 Ibis. . New methods to identify ess in paternity assignment.

: 2195

149 e e in birds. erence high-quality for : 671

14 2212. rs enablers parentage and : microsatellite loci. 176. 692. Proc. R. Soc. B Biol. nference from ). ).

x ratios.

Behav. Ecol. ian modeling e e genetic J. Evol.J. n of ive Mol. ion. This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. Queller, D.C. Sambrook,J., Fritsch, E.F., & Maniatis, T. Krokene, C., Rigstad, K.,Dale, M., & Lifjeld, J.T. Pogány, Á., Dijk, van R.E., Horváth, P. & Székely,T. Pogány, A., Szentirmai, I., Komdeur, J. & Székely, T. Seutin, G., White, B.N. & Boag, P.T. Liker, A., Freckleton, R.P. & Székely, T. Liker, A., Freckleton, R.P. & Székely, T. Sheldon, B.C. Lott, D.F.Lott, Parker,G. Szentirmai, I., Székely, T. & Komdeur, J. Trivers, R.L. Mészáros, L.A., Frauenfelder, N., der van Velde, M., Owens, I.P.F. & Bennett, P.M. Persson, O. & Ohrstrom, P. Valera, F., Hoi, H. & Schleicher, B. Accepted Article ( output in male-only cared and only female- cared cl Annu. Rev. Evol. Ecol. Syst. Penduline Tit, 1557. blue tits blue tits and great tits: good genes or fertility i offspring desertion Eurasianin PendulineTit, DNA analyses.DNA ed.). ed.). Cold Spring Harbour Laboratory Press, Sp Cold skewed adultskewed sex ratios in birds. adult adult sex ratio. 1739 clutch desertion on reproductive success of male an Resour 357 University Press, Cambridge, UK. birds. birds. of manof 1871-1971 45 Polymorphic microsatellite DNA markers in the Pendu Remiz pendulinus : 525 : 341 1991. 1991.

1970. Sperm1970. competition and its evolutionary conseq Proc. R. Soc. B Biol. Sci. 1744. . . 8 Parental1972. investment and sexual selection. In 1997. 1997. Why femalesdo care more than males? 2002. Relating paternity to paternal care. 567. : 692 50. Intraspecific variation in socialthe systems vertebrwild of

Remiz pendulinus Can. J. Zool. Nat. Commun. 694. 694. , pp. 139 ). ). Auk A1989. new avian mating system: ambisexual polyga

129 Mortality1994. costs parental of care and sexual

37 69 179. Aldine179. Publishing Company, Chicago, IL, USA.

: 773 : 43 257 : 82

4 1997. 1997. Egg burial Penduline in Tits, : 1587. 1991. Preservation1991. avianof blood and tissue sample . Curr. Biol. Ornis. Scand.

: 1 : 66. 90. 781. 2014. Divorce2014. and infidelity are associated with 2013. The2013. evolution of sex roles in birds relateis 8.

Sexual2007. conflict over care: antagonistic effe

1987

24 .

1998 Molecular cloning: a laboratory manual

: 880- 20 Remiz pendulinus nsurance?

2012. Parental2012. behavior and reproductive : 105 : Sexual2008. conflict and consistency of Komdeur, J., & Szabad, J. . The function extrapairof paternity in Philos. Trans. R. Soc. Lond. B Biol. Sci. utches utches in the EurasianPenduline Tit 884 d d female penduline tits. ring Harbor, NY, USA. line Tit, line Tit, Proc. R. Soc. B Biol. Sci. 111. . Behav. Ecol. : uences in the insects. Sexual selection and the descent Remiz pendulinus . BMC Evol.BMC Biol. Remiz pendulinus ates.

9 : 649 Cambridge dimorphism in

2008 J. Evol. Biol.

656. my in my the 264

8 . . Mol. Ecol.Mol. : 242.

Biol. Rev. : 1555 , its role, its (2nd s for for s d tod cts cts of

20

: : van Dijk,van R.E., Brinkhuizen, D.M., Székely, T. & Kom This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. van Dijk,van R.E., Komdeur, J., Velde, M., Szentirmai, van Dijk,van R.E., Szentirmai, I., Komdeur, J.Székely & van Dijk,van R.E., Mészáros, L.A., der van Velde, M., Szék van Dijk,van R.E., Pilon, A.E.,Szentirmai, I., Székely, Wang, J. & Santure, A.W. Westneat, D.F. & Sherman, P.W. Williams, G.C. AcceptedYasui, Y. Article Behaviour Eurasian Penduline areTit not related to breeding in mate desertion in mate and female polyandry. pendulinus Székely, T. 96 Komdeur, J care care in Penduline Tits Tit. Tit. habitat habitat structure on sexual conflict over care in P under under polygamy. Behav. Ecol. USA 13 : 3 : : 246 Behav. Sociobiol. Ecol. . The genetic benefits of female multiple mat 11. 250.

1966.

147 . 2008b. Offspring sex ratio in the sequentially pol

J. Ornithol.J. . 4

2010

: 66 : 1551 Adaptation and natural selection Genetics b. Nest desertion is not predicted by cuckoldry in 77. Parentage2009. and sibship inference from multilo

1565. Remiz pendulinus 149

64 181 : 521-527. Parentage1992. and the evolution of parental beha : 1425 : 1579 1435. 1594. : the process of clutch desertion. Behav. Ecol.

T. & Komdeur, J. I., Yang, X., Ffrench-Constant, R. . Princeton University Press, Princeton, NJ, , T. enduline Tits, deur, J. ely, T., Pogány,Á., Szabad, J., densities and mating opportunities. 2007. Sexual2007. conflict over parental

8 : 20 ing reconsidered 2010 27. ygamous Penduline Tit,

a. Parentala. care strategies in Remiz pendulinus

2008 the EurasianPenduline a. The The a. influence of Ibis cus cus genotype data Trends Evol.Ecol. 149 vior. . : 530- & & & & Ardea Remiz 534.

This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. 1. Table Accepted Article Penduline Tit. Remiz- Remiz- Remiz- Locus Remiz- Remiz- Microsatellite characterization the in White-crownedand Cape Penduline Tit 09 07 01 14 10

Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline crowned crowned crowned crowned crowned crowned Species Species White White White White White Cape Cape Cape Cape Cape Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit # individuals # Genotyped Genotyped 168 166 168 148 67 67 67 67 67

range (bp) (bp) range Allele size Allele 206 169 107 206 187 177 108 113 159 214 214 190 269 223 223 211 206 137 168 179

alleles alleles 20 11 3 6 # 9 7 5 9 6

0.23 0.23 0.63 0.29 0.76 0.76 0.78 0.46 0.45 0.37 0.81 Ho

0.23 0.23 0.73 0.75 0.80 0.80 0.77 0.48 0.79 0.74 0.79 He

Estimated frequency frequency null allele nullallele

0.019 0.019 0.005 0.005 0.016 0.064 0.064 0.442 0.026 0.026 0.030 0.269 0.334 This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. Accepted Article CAM- Remiz- Remiz- Locus CAM- CAM- CAM- 10 17 15 13 18 17

Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline crowned crowned crowned crowned crowned crowned Species Species White White White White White Cape Cape Cape Cape Cape Cape Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit # individuals # Genotyped Genotyped 173 168 172 172 167 67 67 67 67

range (bp) (bp) range Allele size Allele 100 142 203 283 215 213 179 183 83 114 114 394 394 164 211 211 385 221 218 187 194

alleles alleles 24 11 9 6 # 5 7 5 4 7

0.85 0.85 0.89 0.78 0.37 0.37 0.85 0.76 0.51 0.43 0.68 Ho

0.80 0.89 0.71 0.39 0.39 0.85 0.77 0.50 0.42 0.72 He

Estimated frequency frequency null allele nullallele 0.034 0.034 0.005 0.042 0.001 0.001 0.005 0.041 0.045 0.045 0.004 0.036 This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. Accepted Article CAM- CAM- CAM- Locus TG01-124 TG01-040 24 20 18

Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline crowned crowned crowned crowned crowned crowned crowned crowned Species Species White White White White White White Cape Cape Cape Cape Cape Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit # individuals # Genotyped Genotyped 149 171 167 64 67 66 67

range (bp) (bp) range Allele size Allele 334 203 396 404 291 198 97 102 102 340 340 204 400 400 406 293 211

alleles alleles 11 4 2 # 2 2 2 3

0.50 0.46 0.28 0.28 0.16 0.35 0.22 0.86 Ho

0.54 0.54 0.49 0.31 0.31 0.18 0.33 0.35 0.83 He

Estimated frequency frequency null allele nullallele 0.037 0.037 0.026 0.041 0.041 0.028 0.040 0.040 0.059 0.208 This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. Accepted Article TG04-041 TG04-012 TG03-098 Locus TG05-053 TG05-053 TG05-046 TG04-061 Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline crowned crowned crowned crowned crowned crowned Species Species White White White White White Cape Cape Cape Cape Cape Cape Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit # individuals # Genotyped Genotyped 173 171 173 173 171 169 67 67 67

range (bp) (bp) range Allele size Allele 137 136 229 233 201 326 188 184 170 145 145 141 230 234 295 295 332 196 195 190

alleles alleles 10 5 3 2 2 # 9 3 4 7

0.64 0.64 0.40 0.58 0.43 0.79 0.79 0.58 0.27 0.67 0.71 Ho

0.67 0.67 0.42 0.50 0.49 0.78 0.78 0.53 0.25 0.77 0.71 He

Estimated frequency frequency null allele nullallele 0.076 0.076 0.013 0.013 0.047 0.065 0.010 0.010 0.013 0.065 0.066 0.066 0.009 This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. Acceptedand estimated null allele frequencies were calculat bp, basepairs; Hoand He represent observed and exp Article TG13-017 TG13-017 TG12-015 TG11-011 Locus

Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline Penduline crowned crowned crowned crowned crowned Species Species White White White White Cape Cape Cape Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit Tit # individuals # Genotyped Genotyped 170 66 67 67

range (bp) (bp) range Allele size Allele 279 210 231 308 281 281 216 240 320 320 ed in CERVUS v (Kalinowski 3.0 ected heterozygosity,ected respectively. Ho, He

alleles alleles 2 4 9 # 4 0.09 0.09 0.64 0.88 0.42 0.42 Ho

0.10 0.10 0.63 0.83 0.43 0.43 He

et al . 2007). Estimated frequency frequency null allele nullallele 0.013 0.013 0.035 0.032 0.032 0.004 0.004 paternal care ( included as a randomterm. Dijk Dijk parentssocial ha

Figure Figure This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. Figure Figure titles effectsFixed Table 2. nest. nest. The Eurasian Penduline Tit data are sourced f identity and the sex of parent(s) provisioning the Acceptedparasitism (IBP) shownare for each species nestlings found to be either within-pair young (WPY Article Species (White-crownedSpecies Penduline Tit) (Eurasian)Species EPP

et al. 2. 1. ( Extra-pair paternity (EPP) variation in threepend Diversity Parameter estimatesParameter and fit statistics theof Bayes 2010 c b). are ve been identified and the Eurasian Penduline Tit dat of or nestling provisioning behaviour abandon

) ) (nat nests = 74) penduline three of tit species. . All data basedare on offspring in where nests both 1.31 -8.19 -1.01 Estimate young post-hatching were recorded at each rom vanrom Dijk ), the result), EPPof or intra-specific brood in three penduline tit species. The 1.94 2.01 0.92 s.e. ian ian GLMM model to predict used uline tit species. The proportion of

et al. (2010b). a are sourcedvan from 0.67 -4.08 - z 1.10

Male ID was 0.50 <0.001 0.27 P

This article is protected by copyright. All rights reserved. This article isprotected rights by All copyright. reserved. AcceptedFigure 2. Article Figure 1. Percentage of young (%) Percentage of nests (%)

0 20 40 60 80 100 0 20 40 60 80 100

Eu Eu ra ra si an an si an an (n =1 (n 8 White 38) =1 66) White-crowned White-crowned 66) Pe nduline Ti Pe nduline nduline Ti -cro Pe wned wned ndulineTi t species t (n species (n =2 =1 9) Cape Cape 9) 8) Cape Cape 8) t species (n =4 2) (n =2 Parentage 1) I EPP W BP PY Pa re

Bi Bi Unipa Unipa ntal pa pa re re ca re re ntal.with.helper ntal ntal. ntal.fe re t ma yp ma e le le