This is a repository copy of Levels of extra-pair paternity are associated with parental care in penduline tits (Remizidae).
White Rose Research Online URL for this paper: http://eprints.whiterose.ac.uk/109970/
Version: Accepted Version
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.
Reuse Unless indicated otherwise, fulltext items are protected by copyright with all rights reserved. The copyright exception in section 29 of the Copyright, Designs and Patents Act 1988 allows the making of a single copy solely for the purpose of non-commercial research or private study within the limits of fair dealing. The publisher or other rights-holder may allow further reproduction and re-use of this version - refer to the White Rose Research Online record for this item. Where records identify the publisher as the copyright holder, users can verify any specific terms of use on the publisher’s website.
Takedown If you consider content in White Rose Research Online to be in breach of UK law, please notify us by emailing [email protected] including the URL of the record and the reason for the withdrawal request.
[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 birds 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 tit (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, passerine 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 Penduline Tit 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 Eurasian Penduline Tit 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, Remiz 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 Cape Penduline Tit 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, South Africa (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 Animal the by approved were Tits Penduline stored in 1 1 in stored Accepted Article
nhsou minutus Anthoscopus , van Dijk Dijk van , , van Dijk Dijk van ,
ml of Queen s 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 bird 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