Jul 18, 1994 - 1 Museum of Natural Science, 119 Foster Hall, Louisiana State. University ..... Sall J, Ng K, Hecht M (1991) JMP user's guide. SAS Institute ...
Behav Ecol Sociobiol (1995) 37:103-108
© Springer-Verlag 1995
Linda A. Whittingham • Jan T. Lifjeld
High paternal investment in unrelated young: extra.pairpaternity and maleparentalcare in housemartins
Received: 18 July 1994/Accepted after revision: 1 April 1995
Abstract The response of males to reduced paternity has important consequences for the evolution and maintenance of a mixed reproductive strategy. Paternity is predicted to affect directly the level of male parental care in some cases but not in others. The response of males to reduced paternity will be influenced by their ability to assess their paternity, the predictability of cuckoldry and the costs and benefits of parental care. Although male house martins (Delichon urbica) provide among the highest levels of male parental care known in passerines (incubation, brooding and feeding nestlings), there was no evidence that cuckolded males substantially reduced their level of parental care, and, as a result, all young fledged successfully. Thus, extra-pair fertilizations enhanced the reproductive success of some males because they were able to parasitize the parental care of cuckolded males. We discuss several conditions which may favor extensive male parental care even when the male's paternity is very low. Key words Parental care • Extra-pair paternity •
Delichon urbica
Introduction
In most species of birds, nestlings require some male parental care to reach independence (Lack 1968). The success of males pursuing a mixed reproductive strategy will depend on both the parental care males pro-
L. A. Whittingham ([])1 . j. T. Lifjeld Zoological Museum, University of Oslo, Sarsgt. 1, N-0562 Oslo, Norway Present address:
1 Museum of Natural Science, 119 Foster Hall, Louisiana State University, Baton Rouge, LA 70803-3216, USA
vide to the young they have sired in their own nest and their ability to parasitize the parental care of other male's that are raising their extra-pair young. Parental care is a costly part of reproduction (Williams 1966; Askenmo 1979; Grafen 1980), and as a result, natural selection should favor males that avoid caring for unrelated young (Trivers 1972). However, recent studies have shown that male parental care often does not vary in relation to paternity (reviewed in Whittingham et al. 1993; but see Weatherhead et al. 1994). As a result, some males contribute a substantial amount of parental care toward raising another male's offspring. A major consequence of this behavior is that a mixed reproductive strategy can be maintained. The effect of paternity on the level of male parental care will depend on several factors including, the ability of males to assess their paternity, the predictability of cuckoldry and the costs and benefits of male parental care (Whittingham et al. 1992; Westneat and Sherman 1993). Costs are generally evaluated in terms of future survival or fecundity and lost additional mating opportunities. Thus, costs are likely to depend on the extent of male parental care. Research examining the effect of paternity on male parental care has thus far focused primarily on species of birds where male parental care consists only of feeding young (reviewed in Whittingham et al. 1993; but see Weatherhead et al. 1994). However, in birds, feeding young is only one aspect of parental care, and in species in which males invest heavily in other forms of parental care (including courtship feeding, incubation and brooding as well as feeding young) selection may be more likely to favor more accurate means of assessing paternity. Can extra-pair fertilizations be an effective mating tactic in a species with very high levels of male parental care ? Or do males reduce their parental care in relation to their paternity and, consequently, reduce the expected reproductive gains of extra-pair males ? We studied these questions in a small colony of
104 socially m o n o g a m o u s h o u s e m a r t i n s (Delichon urbica). I n this species, the sexes p r o v i d e a n e q u a l share o f incub a t i o n , b r o o d i n g a n d feeding o f nestlings ( C r a m p 1988), thus, p r o v i d i n g a m o n g the highest levels o f m a l e p a r e n t a l care k n o w n a m o n g passerines (Silver et al. 1985).
Methods House martins are small (20 g), sexually monomorphic and monochromatic birds, similar to other members of the family Hirundinidae (Bryant 1989; Turner and Rose 1989). House martins breed throughout Europe in the summer and migrate to Africa, south of the Sahara, in the winter (Cramp 1988). During the breeding season, they nest colonially in socially monogamous pairs (Cramp 1988). Both sexes contribute to nest building, incubation, brooding and feeding nestlings (Cramp 1988). We studied a small colony of house martins breeding in an alpine valley at Ovre Heimdalsvatn, Valdresflya, Norway (61°25'N, 8°52'E) in 1992. In our study area, house martins built mud nests within artificial nest cups (provided in excess) which permitted us easy access to eggs and nestlings. Nests were arranged linearly under the eaves of our cabin and the edge of each nest nearly touched the edges of neighboring nests. We caught all individuals in mist nets at the colony during incubation and each adult was ringed and individually color-marked with acrylic paint on the wings and tail or with permanent felt-tip markers on the rump. We sexed all birds according to the development of a brood patch (most pronounced in females; Bryant 1975). We collected blood samples from adults and nestlings for DNA fingerprinting. There were no cases of brood reduction and all young that hatched were sampled. In the alpine region the breeding season is short and all pairs were single brooded. Average clutch size was 4.3 (_+ 0.2 SE) and average fledging success was 3.8 (+ 0.3). The difference between clutch size and fledging success was due to eggs that did not hatch and showed no signs of embryonic development. We conducted behavioral observations at ten nests during the incubation and nestling periods. Observation sessions began on 22 June and continued through 14 July. We recorded house martin activities every day (except 10 July) for eight 30-rain periods each day, distributed evenly between 0700hours and 1800hours. Hatchdate (day 0) ranged from 27 June to 3 July. Thus, the behavior of individuals at each nest was observed from 6-14 d before hatching until nestlings were 11-15 days old. We watched all nests simultaneously. We recorded (to the nearest second) the time that each adult entered or left the nest cavity. This method allowed us to measure several variables: the amount of time the male, female or both attended the eggs or nestlings (i.e., incubating or brooding), the amount of time eggs or nestlings were left unattended, and the rate at which males and females delivered food to their young. To avoid pseudoreplication, we used mean values in our analyses of behavioral data. For example, we determined an average food delivery rate for each male by averaging the number of food deliveries over the eight 30-min observation periods each day and all days of observation. Means are presented with their SEs. We tested all data for normality with the Shapiro-Wilk test (Sall et al. 1991) and used nonparametric tests for data that were not normally distributed. Details of the DNA fingerprinting methods used in this study are found in Whittingham and Lifjeld (in press) and Lif~eld et al. (1993). Briefly, 6 gg of DNA per individual was digested with Hae III, run through an agarose gel, transferred by Southern blotting onto Hybond-Nfp membranes and hybridized with the 33.15 minisatellite probe (Jeffreys et al. 1985). We used the presence of bands
not found in either parent (novel fragments) and band-sharing coefficients (Wetton et al. 1987) to determine parentage. We considered individuals with three or more novel fragments to be unrelated to one or both putative parents, and we used band-sharing values to determine which putative parent was unrelated to the mismatched young (see Fig. 1, in Whittingham and Lif~eld in press). We considered nestlings to be sired by extra-pair males when they had at least three novel fragments and they shared a high proportion of their bands with their putative mother and a relatively low proportion of their bands with their putative father (Whittingham and Lifjeld in press).
Results Patterns of Parental Care A m o n g pairs, p a r e n t a l duties were s h a r e d equally by the m a l e a n d female. M a l e s t e n d e d a n d i n c u b a t e d eggs 51.6 + 0 . 1 % o f the time, b r o o d e d nestlings 51.7 + 0 . 1 % o f the time, a n d p r o v i d e d 51.3 + 0 . 1 % o f the feeding visits to nestlings (n = 10 nests). T h e time spent i n c u b a t i n g o r t e n d i n g eggs e a c h d a y b y males ( P e a r s o n c o r r e l a t i o n r = 0.07, P > 0.8, n = 12 days) o r b o t h p a r e n t s t o g e t h e r (r = - 0 . 5 0 , P > 0.09, n = 12 days) did n o t c h a n g e significantly over the last 12 days o f the i n c u b a t i o n period. However, the time t h a t eggs were u n a t t e n d e d decreased significantly (r = - 0 . 5 9 , P = 0.045, n = 12 days) closer to the h a t c h ing date a n d this was associated with a significant increase in the time t h a t females spent i n c u b a t i n g (r = 0.68, P = 0.02, n = 12 days). Thus, m a l e p r e - h a t c h ing p a r e n t a l care was similar t h r o u g h o u t the i n c u b a t i o n p e r i o d whereas female p a r e n t a l care increased as eggs a p p r o a c h e d hatching. T h e time spent t e n d i n g eggs by male, female, b o t h p a r e n t s together, o r the total time eggs were u n a t t e n d e d did n o t differ a m o n g the eight t i m e - o f - d a y categories ( A N O V A , df= 7, 72; all F < 1.1, all P > 0.2). N e s t l i n g age ( h a t c h i n g to 14 days old) h a d the greatest effect o n p a r e n t a l care. As nestlings grew o l d e r : 1. B o t h m a l e ( P e a r s o n c o r r e l a t i o n r = 0.94, P = 0.0001, n = 10days) and female (r = 0.95, P = 0.0001, n = 14 days) feeding rate increased (Fig. la). 2. T h e time spent b r o o d i n g nestlings by males (r = - 0 . 8 9 , P = 0.0001, n = 14 days), females (r -- - 0 . 8 2 , P = 0.0002, n = 1 4 d a y s ) o r b o t h p a r e n t s t o g e t h e r (r = - 0 . 7 6 , P = 0.0011, n = 14 days) decreased. 3. T h e a m o u n t o f time nestlings were left u n a t t e n d e d (r = 0.8 8, P = 0.0001, n -- 14 days) increased (Fig. lb). A l t h o u g h feeding rates increased linearly with nestling age (Fig. la), b r o o d i n g time was related curvilinearly to nestling age (Fig. lb). P a r e n t s divided b r o o d i n g time equally a n d nestlings were a t t e n d e d a l m o s t c o n t i n u o u s l y f r o m h a t c h i n g to 8 days o f age, at w h i c h p o i n t the time t h a t nestlings were left u n a t t e n d e d increased d r a m a t i c a l l y (Fig. lb). N e i t h e r b r o o d size ( A N O V A , dr= 3, 6; all F < 3.5, all P > 0.1) n o r time
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48 Nestling age (days)
Fig. la The average number of feeding visits made to the brood by male and female parents in relation to nestling age (day 0 = hatching) b The amount of time male and female parents spent tending and brooding nestlings, and the time nestlings were unattended in relation to nestling age (day 0 = hatching) of day (ANOVA, df= 7, 72; all F < 0.5, all P > 0.42) affected feeding rates to nestlings, or the a m o u n t of time the male, female, or both parents together brooded nestlings, or the a m o u n t of time nestlings were unattended. Extra-pair paternity During the 1992 breeding season there were 11 active nests (Whittingham and Lit]eld in press) and we made intensive behavioral observations at 10 of those nests. Here, we focus on the D N A fingerprinting results for those ten nests. Of 38 nestlings, 11(29%) in six of ten broods (60%) were not the offspring of the putative father. Within broods, the proportion of extra-pair young in each nest varied from 0-75%; thus, each male had sired at least one offspring in the nest that he attended (Whittingham and Lifjeld in press). All young were the genetic offspring of their putative mother (Whittingham and Lifjeld in press).
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% Extra-pairyoung Fig. 2 The percent of extra-pair young in a male's brood in relation to: a % male feeding visits to nestlings, b % time males spent incubating eggs, and e % time males spent brooding nestlings Male parental care and paternity Although the level of male parental care is high in house martins, neither the percentage of male feeds to nestlings (Spearman rank correlation rs = - 0 . 3 1 , P = 0.36, n = 10; Fig. 2a), the percentage of time males spent incubating eggs (rs = - 0 . 0 1 , P = 0.97, n --- 10; Fig. 2b), nor the percentage of time males spent brooding nestlings (rs = 0.025, P = 0.94, n = 10; Fig. 2c) were significantly related to the percentage of unrelated young in the brood. However, males may not be able to perceive their exact level of paternity in the brood, and so we compared the level of parental care for cuckolded and non-cuckolded males. Similarly, the percentage of male feeds to nestlings (50 + 1% cuckolded, 53 + 1% non-cuckolded; Mann-Whitney U = 18, P = 0.20, n = 6, 4), time males spent incubating eggs (52 + 2% cuckolded, 51 + 2% non-cuckolded; U = 13, P = 0.83, n = 6, 4), and time males spent brooding
106 nestlings (51 + 2% cuckolded, 53 + 2% non-cuckolded; U = 1 5 , P = 0 . 5 2 , n = 6 , 4 ) were not significantly different for males that were or were not cuckolded. Although the average level of male parental care was not affected significantly by the male's paternity within the brood, males that provided care to unrelated young may have been more variable or less consistent in their parental duties. However, for both sexes, the variance in feeding visits to nestlings, time spent incubating, and time spent brooding were similar between nests with and without extra-pair young (variance ratio tests, all F < 3.6, all P > 0.1).
We did not find a significant relationship between any measure of male parental care and paternity. Jamieson et al. (1994) also found no significant relationship between male parental care and paternity in a species with similarly high levels of male parental care. Although our sample size was small and male feeding effort showed a slight tendency to decrease with paternity (Fig. 2a), there was virtually no difference between cuckolded and non-cuckolded males for three different measures of paternal care. Despite the low statistical power of our analyses, the minuscule differences (maximum of 3 %) in mean levels of parental care between cuckolded and non-cuckolded males suggest that any effect of paternity on male parental care is likely to be very small, at best. Therefore, it is clear that extra-pair fertilization is a successful reproductive strategy for some house martin males because extra-pair males can parasitize the parental care of other males. Why do cuckolded males contribute a substantial amount of parental care toward raising unrelated young ? Recent theoretical work focusing on the relationship between paternity and male parental care suggests that there are three main factors which will determine whether males will adjust their effort in response to their paternity in a brood (Whittingham et al. 1992; Westneat and Sherman 1993): (1) the availability to males of information on paternity, (2) variation in the risk of cuckoldry among breeding attempts, and (3) the reproductive trade-offs involved in increasing or decreasing parental care. Below we discuss how these factors influence the relationship between parental behavior and paternity in birds and house martins in particular.
behavioral responses to changes in paternity (Westneat and Sherman 1993). The ability to discriminate between related and unrelated individuals within a brood has apparently not evolved in birds (Beecher 1988). This idea is supported by a detailed study on pied flycatchers (Ficedula hypoleuca) which showed that parents do not preferentially feed related young even when they differed in size from unrelated young (Lit]eld et al. 1992). We think it is more likely that males can estimate their overall probability of paternity for a brood even though they cannot discriminate between related and unrelated individuals within a brood. If this is the case, then it would be possible for males to reduce their parental care in response to reduced paternity in a general way, but not on a individual basis to particular young within the brood. There is experimental evidence that males can estimate their probability of paternity within a brood by the amount of time they spend with the female during her fertile period. Temporary male-removal experiments during the female's fertile period have shown that male dunnocks (Prunella modularis) respond to a reduced probability of paternity by feeding nestlings less frequently (Hatchwell and Davies 1990) and male acorn woodpeckers (Melanerpes forrnicivorus)respond by destroying the nest and eggs, forcing the female to renest (Koenig 1990). If males can estimate their paternity within a brood, should the level of paternal care be adjusted proportionately ? If males cannot recognize and preferentially care for unrelated young, and nestling survival is dependent on male parental care, then a reduction in paternal care will negatively affect related as well as unrelated young. In communal breeders (e.g., dunnocks and superb fairy-wrens, Malurus cyaneus) other individuals will compensate for a reduction in male parental care, and, therefore, survival of neither related nor unrelated young is affected adversely when males reduce parental care in proportion to their perceived paternity (Hatchwell and Davies 1990; Mulder et al. 1994; but see Jamieson et al. 1994). However, this will not necessarily be the case in socially monogamous species with biparental care because in most cases the female cannot compensate completely for reductions in male parental care (Houston and Davies 1985; Wolf et a1.1988; Bart and Tornes 1989; Dunn and Hannon 1989). Thus, similar to other monogamous biparental species (reviewed in Whittingham et al. 1993), house martin males did not reduce their level of parental care in relation to paternity.
Male assessment of paternity
Variation in the risk of cuckoldry
If males are unable to gather or process information which enables them to assess their paternity, then they cannot adjust their parental care accordingly. If this is the case, then we would never expect short term
Another way in which males could estimate their paternity within a brood is if the risk of cuckoldry varies among broods in a predictable rather than random manner (Westneat and Sherman 1993). If this is the
Discussion
107
case, then males might be able to adjust their parental care in relation to their paternity. In support of this idea, Morton et al. (1990) found that yearling purple martins (Progne subis) had lower paternity and fed nestlings less often than did older males. However, there is evidence from other species that paternity does not vary predictably with age or breeding experience. Dunn et al. (1994) followed the paternity of individual tree swallows through two or three breeding seasons, and found no consistent trends in paternity. Future studies examining the relationship between paternity and male parental care will need to determine whether paternity varies predictably within seasons (e.g., multiplebrooded species) and among seasons for the same individuals. If paternity does not vary predictably, then the dilemma for cuckolded males is that they risk the death of related young if they reduce their parental care to the brood. Thus, the question becomes, when should a male reduce parental care in relation to paternity and risk the death of related young ? Reproductive trade-offs If males can assess roughly their paternity within a brood and their level of paternity varies randomly, then the level of parental care should vary with paternity in relation to the costs and benefits of providing that care. In general, the benefit is the increased likelihood that related young will survive if the whole brood (including unrelated young) receives the male's parental care. We expect this is the case in species of birds where extra-pair paternity is common, otherwise males should forgo parental care completely. Alternatively, the costs of parental care can be the reduced probability of survival of the male parent to the next breeding season or missed opportunities for additional matings (e.g., polygyny or extra-pair fertilizations; Grafen 1980; Whittingham et al. 1992). For house martins studied in Scotland, Bryant (1988) showed that birds provisioning nestlings with more food expended more energy; however, there was no evidence that greater energy expenditure translated directly into a survival cost. Additional mating opportunities include the attraction of additional pair-mates as well as gaining extrapair fertilizations, although the latter is more widespread in birds and therefore more likely to influence male parental care. The frequency of extrapair paternity in many species of socially monogamous birds (reviewed in Westneat and Webster 1994), suggests that a cost in terms of lost extra-pair fertilizations may be incurred by males spending their time and energy feeding mixed broods of related and unrelated young. If female fertile periods occur asynchronously due to predation or multiple brooding, then males can potentially incur a reproductive cost from missed extra-
pair fertilization opportunities throughout the nesting cycle. A trade-off between feeding nestlings and extrapair fertilizations is unlikely to influence house martin behavior in our population, because there was no predation and the breeding season was very short and synchronous. As a result, female fertile periods did not overlap with nestling periods. However, a trade-off between male parental care and extra-pair fertilizations may be important in species of birds with longer breeding seasons, multiple brooding and renesting due to predation. The recent attention to the relationship between paternity and male parental care is due primarily to the advent of molecular techniques which allow us to examine the genetic relatedness between young and their putative parents. This is an area in which there is a tremendous amount of work yet to be done. We suggest future studies of paternity and parental care focus initially on examining the information available to males for paternity assessment, whether paternity varies predictably within and among seasons, and if there is a cost of parental care in terms of missed mating opportunities or reduced survival of nestlings or adults. Recent models predict that male parental care should vary positively in relation to paternity in some cases but not in others (Whittingham et al. 1992; Westneat and Sherman 1993). It is imperative that we investigate both the assumptions and predictions of these models if we are to be successful in describing the evolution and maintenance of both mixed reproductive strategies and male parental care in birds. Acknowledgements We thank Alec Jeffreys for supplying the minisatellite probe and John E. Stacy for assistance with the hybridization procedure. Peter Dunn, Patty Gowaty, Bob Montgomerie and an anonymous reviewer provided helpful comments on the manuscript. This research was supported by a grant from the Norwegian Research Council to the DNA lab at the Department of Biology, University of Oslo, and a postdoctoral fellowship from the American Scandinavian Foundation to L.A.W.
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108 Dunn PO, Hannon SJ (1989) Evidence for obligate male parentalcare in black-billed magpies. Auk 106:635-644 Dunn PO, Whittingham LA, Lifjeld JT, Robertson RJ, Boag PT (1994) Effects of breeding density, synchrony, and experience on extrapair paternity in tree swallows. Behav Ecol 5:123-129 Grafen A (1980) Opportunity cost, benefit and degree of relatedness. Anim Behav 28:967 968 Hatchwell BJ, Davies NB (1990) Provisioning of nestlings by dunnocks, Prunella modularis, in pairs and trios: compensation reactions by males and females. Behav Ecol Sociobiol 27:199-210 Houston AI, Davies NB (1985) The evolution of cooperation and life history in the Dunnock Prunella modularis. In: Sibley, R, Smith, R (eds) Behavioural ecology: the ecological consequences of adaptive behaviour. Blackwell, Oxford, pp 471-487 Jamieson IG, Quinn JS, Rose PA, White BN (1994) Shared paternity among non-relatives is a result of an egalitarian mating system in a communally breeding bird, the pukeko. Proc R Soc Lond B 257:271-277 Jeffreys AJ, Wilson V, Thein SL (1985) Individual-specific "fingerprints" of human DNA. Nature, 316: 76-79 Koenig WD (1990) Opportunity of parentage and nest destruction in polygynandrous acorn woodpeckers, Melanerpes form# civorus. Behav Ecol 1 : 55-61 Lack D (1968) Ecological adaptations for breeding in birds. Methuen, London Lifjeld J T, Breiehagen T, Lampe H M (1992) Pied flycatchers failed to use nestling size as a cue to favour own genetic offspring in a communally raised brood. Ornis Scand 23:199-201 Lifjeld JT, Dunn PO, Robertson RJ, Boag PT (1993) Extra-pair paternity in monogamous tree swallows. Anim Behav 45: 213-229 Morton ES, Forman L, Braun M (1990) Extrapair fertilizations and the evolution of colonial breeding in purple martins. Auk 107: 275~83 Mulder RA, Dunn PO, Cockburn A, Lazenby-Cohen KA, Howell MJ (1994) Helpers liberate female fairy-wrens from constraints on extra-pair mate choice. Proc R Soc Lond B 255:223-229
Sall J, Ng K, Hecht M (1991) JMP user's guide. SAS Institute, Cary Silver R, Andrews H, Ball G F (1985) Parental care in an ecological perspective: a quantitative analysis of avian subfamilies. Atn Zool 25 : 823-840 Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldine, Chicago, pp 136-179 Turner A, Rose C (1989) Swallows and martins. Houghton Mifflin, Boston Weatherhead PJ, Montgomerie R, Gibbs HL, Boag PT (1994) The cost of extra-pair fertilizations to female red-winged blackbirds. Proc R Soc Lond B 258:315-320 Westneat DF, Sherman PW (1993) Parentage and the evolution of parental behavior. Behav Ecol 4:66-77 Westneat DF, Webster MS (1994) Molecular analyses of kinship in birds: Interesting questions and useful techniques. In: DeSalle R, Wagner GP, Shierwater B, Streit B (eds) Molecular approaches to ecology and evolution. Birkhauser, Basel Wetton JH, Carter RE, Parkin DT, Walters D (I 987) Demographic study of a wild house sparrow population by DNA fingerprinting. Nature 327 : 147-149 Whittingham LA, Taylor PD, Robertson RJ (1992) Confidence of paternity and male parental care. Am Nat 139:1115-1125 Whittingham LA, Dunn PO, Robertson RJ (1993) Confidence of paternity and male parental care: an experimental study in tree swallows. Anita Behav 46:13%147 Whittingham LA, Lifjeld JT (in press) Extra-pair paternity increases the opportunity for sexual selection in the monogamous and monomorphic house martin. J Avian Biol Williams G (1966) Natural selection, the costs of reproduction, and a refinement of Lack's principle. Am Nat 100:687-690 Wolf L, Ketterson ED, Nolan Jr. V (1988) Paternal influence on growth and survival of dark-eyed junco young: do parental males benefit? Anim Behav 36:1601 1618 C o m m u n i c a t e d b y R. M o n t g o m e r i e
