Measurement of heritability of hatching date and chick condition in parasitic jaegers

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1 2290 Measurement of heritability of hatching date and chick condition in parasitic jaegers R.A. Phillips and R.W. Furness Abstract: There are few published studies of heritability of reproductive traits in long-lived birds. In parasitic jaegers (Stercorarius parasiticus) breeding on Foula, Shetland, there was no significant heritability in calendar hatching date or relative hatching date, using either mother offspring, father offspring, or pooled mother/father offspring regressions. By contrast, chick body condition (mass corrected for size) was highly heritable. Both traits were important determinants of chick survival from banding until recruitment. High heritability of chick condition was therefore surprising, as characters closely related to fitness are generally assumed to have low heritability. However, chick condition may include a component of structural size, and morphological traits tend to have high heritabilities despite frequently having an important influence on fecundity or viability in birds. Résumé : Il existe peu de travaux publiés sur l héritabilité des caractères relatifs à la reproduction chez les oiseaux qui vivent longtemps. Chez des Labbes parasites (Stercorarius parasiticus) qui se reproduisent dans l île de Foula, Shetland, les régressions mère rejetons, père rejetons, ou mère/père rejetons n ont pas révélé d héritabilité significative de la date d éclosion réelle ou de la date relative de l éclosion. En revanche, le coefficient de condition (masse pondérée d après la taille) des oisillons s est avéré fortement héritable. Les deux caractéristiques sont d importants facteurs déterminants de la survie des oisillons entre le moment où ils sont bagués et le recrutement. La forte héritabilité de la condition des oisillons est par conséquent plutôt surprenante, puisque les caractéristiques fortement reliées au fitness sont généralement considérées comme de faible héritabilité. Il faut cependant se rappeler que la condition des oisillons peut comporter une composante de taille structurale et que les caractéristiques morphologiques ont tendance à être fortement héritables, même si elles ont souvent une forte influence sur la fécondité ou la viabilité chez les oiseaux. [Traduit par la Rédaction] Notes 2294 Introduction Obtaining the data necessary to determine heritability of different characters in populations of wild birds can be a laborious process (Boag and van Noordwijk 1987); in particular, there are few values for species that defer breeding for many years. As an alternative, researchers frequently calculate the repeatability value of a trait, which in theory sets the upper limit to heritability (Falconer 1989). Although these approaches yield similar results in some populations, this is not always the case (Boag and van Noordwijk 1987). Repeatability is normally greater, because it measures the fraction of phenotypic variance in a character resulting from permanent, or nonlocalised, differences between individuals, which includes both genetic and environmental effects, whereas heritability estimates the fraction that can be attributed to additive genetic variance only (Boag and van Noordwijk 1987). Received May 20, Accepted August 31, R.A. Phillips 1 and R.W. Furness. Applied Ornithology Unit, Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow, G12 8QQ, United Kingdom. 1 Author to whom all correspondence should be sent at the following address: Wildfowl and Wetlands Trust Caerlaverock, Caerlaverock, Dumfries, DG1 4RS, United Kingdom ( Can. J. Zool. 76: (1998) Repeatabilities of two important reproductive traits, laying date and chick condition (mass corrected for size), were low to moderate in established pairs of parasitic jaegers (Stercorarius parasiticus) breeding on Foula, Shetland, in (Phillips and Furness 1998). This is one of the few seabirds for which there is also a published value for heritability of laying date, from a long-term study of jaegers breeding at Fair Isle, also in Shetland (O Donald 1983). However, this latter value (0.85) exceeded repeatability in the Foula population and is considerably higher than heritability recorded in other bird species, which is generally 0.4 or less (Newton and Marquiss 1984; Gustafsson 1986; Perdeck and Cavé 1992; Hakkarainen et al. 1996). Furthermore, hatching date (and also chick growth rate and fledging mass) shows strong relationships with postfledging survival in seabirds (Nisbet and Drury 1972; Perrins et al. 1973; Spear and Nur 1994). These traits are clearly important components of overall fitness and, as such, would generally be expected to exhibit comparatively low heritability (Fisher 1930). This study therefore examines the heritability of hatching date and chick condition and discusses their relationship with fitness in the Foula population of parasitic jaegers. Methods Heritability estimates Mass and wing-length (maximum wing chord) measurements were available for large numbers of parasitic jaeger chicks that had

2 Notes 2291 Fig. 1. Relative hatching dates (days relative to the mean in each year) of parasitic jaeger chicks on Foula in and the relative hatching date of their parent. been banded on Foula, Shetland (60 08 N, 2 05 W), each year between 1976 and Between 1992 and 1994, 29 of these birds were trapped and color-banded as breeding adults on Foula. The hatching date, relative hatching date, and chick body condition index for these birds were calculated from their measurements as chicks, as follows. Hatching date was estimated from wing length on the basis of a logistic curve fitted to wing length versus age for chicks of known age in 1992 (Phillips et al. 1996). The very slight variation among years in wing growth had a negligible effect on the estimation of hatching date (Phillips et al. 1996), consequently the error associated with this approach can be assumed to be minor. Relative hatching date was estimated by comparison with the mean hatching date in each year. An index of chick body condition was calculated as the deviation of observed from expected mass at a particular age, expressed as a proportion of the expected value (following Bolton 1995; Phillips et al. 1996). Expected mass was obtained from the equation of a logistic curve fitted to mass versus age for chicks of known age in During , hatching dates of chicks of the color-banded birds were established by direct observation (territories were visited daily or on consecutive days around the time of hatching). Most chicks were also weighed and measured on one to four occasions during chick rearing, and an index of body condition (a mean value if more than one measurement was available) was calculated as before. To maintain statistical independence, the mean values for chick hatching date and chick body condition index of all offspring of each color-banded bird between 1992 and 1994 were used in the following analyses. Heritability (h 2 ) can be estimated from the slope of the regression of offspring versus mean parental value or, more commonly, twice the slope of the offspring value regressed on that for one parent (Falconer 1989). Frequently, only mother offspring heritabilities are calculated for reproductive traits. However, in parasitic jaegers, both parents feed the chick and presumably influence its body condition. Furthermore, repeatability in laying date of male parasitic jaegers that changed mate was significantly higher than in females that did so, and laying date was related to male rather than female body condition (Phillips and Furness 1998). This suggests that a male characteristic (presumably his ability to provide sufficient food to get his partner into reproductive condition) is important in determining the timing of breeding. Both mother offspring and father offspring regressions were therefore carried out, in addition to pooled mother/father offspring regressions (to maximise sample sizes and include some unsexed adults). We were unable to sex offspring and, because of reversed size dimorphism in this species, this may increase the error in heritability estimates for chick condition, but would be unlikely to have any effect on the overall conclusions. One-tailed probabilities are presented, as we are testing the hypothesis that offspring resemble their parent (e.g., Perdeck and Cavé 1992; Hochachka 1993). Heritabilities are generally calculated from values measured at the same stage in all individuals, because, for example, chick condition may vary seasonally or laying date may change with adult age. Repeatability of body condition was, however, quite high (r i = 0.53, p < ) in a sample of 467 chicks measured more than once during chick rearing on Foula in , indicating that, relative to others, each individual maintains a reasonably consistent level of condition throughout the nestling period. Although chick body condition shows no significant relationship with parental age, laying date changes with age in parasitic jaegers, with birds in the youngest age category (5- to 8-year-olds) laying significantly later than mid-aged or older adults (Phillips 1995); however, excluding the youngest age group had no effect on the results (analyses are not presented). Consequently, while it may add some statistical noise, the influence of measuring traits in birds of different ages on our conclusions was assumed to be minor. Timing of breeding, chick growth, and survival In addition to the 29 adults trapped on Foula, another 9 birds banded as chicks in previous years were recorded at Shetland colonies 4 years or more after they fledged (British Trust for Ornithology banding recoveries data base). These were probably breeding birds, as parasitic jaegers in Shetland generally recruit at 4 or 5 years of age (O Donald 1983). The growth and hatching dates of the 38 recruits (less than 3% of the total) were compared with those of the remaining chicks that were not known to have survived and recruited at any colony. To normalise the data, chick body condition and hatching date were square-root transformed and relative hatching date was inverse transformed before analysis. Results Heritability estimates The estimated heritability (mean ± SE) of calendar hatching date and relative hatching date were 0.22 ± 0.72 (r 2 = 0.01, n = 16, p = 0.38) and 0.70 ± 0.72 (r 2 = 0.06, n = 16, p = 0.17) from the father offspring mean regression, 0.21 ± 0.44 (r 2 = 0.03, n = 10, p = 0.68) and 0.20 ± 0.50 (r 2 = 0.02, n = 10, p = 0.65) from the mother offspring regression, and 0.02 ± 0.44 (r 2 = 0.00, n = 29, p = 0.48) and 0.27 ± 0.49 (r 2 = 0.01, n = 29, p = 0.29 from the pooled father/mother offspring regression, respectively (Fig. 1). None of these regressions was statistically significant and confidence limits were clearly very wide. Estimated heritability of chick condition, however, was high and statistically significant from the father offspring regression, with h 2 = 1.57 ± 0.66 (r 2 = 0.30, n = 15, p < 0.02), from the mother offspring regression, with h 2 = 0.92 ± 0.25 (r 2 = 0.65, n =9, p < 0.005), and from the pooled father/mother offspring regression, with h 2 = 1.03 ± 0.25 (r 2 = 0.40, n = 27, p < ) (Fig. 2).

3 2292 Can. J. Zool. Vol. 76, 1998 Table 1. The mean chick-condition index and hatching dates of parasitic jaeger chicks banded on Foula between 1976 and 1989 in relation to their fate. Status Chick condition index Hatching date Relative hatching date Recruited a 0.03±0.11 (38) 49.7±5.4 (38) 1.37±4.7 (38) Unknown 0.02±0.11 (1275) 52.0±5.7 (1298) 0.04±5.1 (1298) t test t 1311 = 2.91, p = t 1334 = 2.65, p = t 1334 = 1.74, p =0.08 Note: Values are presented as untransformed means (± 1 SD), but data were transformed before analysis (see Methods). Numbers in parentheses are sample sizes. a Birds aged over 4 years that were trapped or recovered at any Shetland colony. Influence of hatching date and chick body condition on juvenile survival Differences in hatching date and body condition made a significant contribution to variation in overall fitness (Table 1). Birds that were known to have recruited into Shetland colonies had grown significantly better as chicks than those of unknown fate. Although they did not hatch significantly earlier relative to the mean in their particular year (p = 0.08), on average they did hatch on earlier calendar dates, i.e., without correcting for annual variation. In a stepwise logistic regression with all three variables available for entry, the probability of recruitment was related to both chick condition and calendar hatching date (chick condition: Wald s statistic = 11.7, p < 0.001; hatching date: Wald s statistic = 8.2, p < 0.005). With calendar hatching date unavailable for entry, the probability of recruitment was related to chick condition and relative hatching date (chick condition: Wald s statistic = 10.4, p < 0.005; relative hatching date: Wald s statistic = 4.2, p < 0.05), even though for the latter the univariate analysis showed no significant difference between the two groups. Fig. 2. Body condition index (mass corrected for age) of parasitic jaeger chicks on Foula in and chick condition index of their parent. The regression line relates to the pooled data set. Discussion In this study, the estimates of heritability were very low and nonsignificant for calendar hatching date and generally higher but still nonsignificant for relative hatching date, irrespective of whether mother offspring, father offspring, or pooled father/mother offspring regressions were considered. This compares with the high heritability value for laying date recorded in the previous study on Fair Isle from a smaller sample of 22 parasitic jaegers (O Donald 1983). As outlined in the Introduction, this last number is probably an overestimate. Heritability values obtained in separate years or from separate study populations of great tits (Parus major) also showed poor agreement, reflecting differences in environmental conditions and, to some extent, the influence of outlying values in analyses (van Noordwijk 1987; Gebhardt-Henrich and van Noordwijk 1991). By contrast, on Foula there appeared to be significant and high heritability of chick body condition, although, as with hatching dates, the exact values are unreliable because of the large standard errors. Heritability appears to exceed the repeatability of a related trait, mean chick body condition in two-chick broods, which was 0.43 in a much larger sample of color-banded birds breeding on Foula in (Phillips and Furness 1998). However, this is not unusual, as heritability estimates have exceeded repeatability values or unity in several other studies (e.g., Gebhardt-Henrich and van Noordwijk 1991; Wiggins 1991; Potti 1993; Cooke et al. 1995; Hakkarainen et al. 1996). High heritabilities may be attributable to maternal effects, genotype environment interactions, or a common environment component, if developmental and living conditions of parents and offspring are similar, although the results of field studies that have examined these effects suggest that their influence tends to be comparatively minor (van Noordwijk et al. 1980; van Noordwijk 1987; Wiggins 1989; Cooke et al. 1995; but see Schluter and Gustafsson 1993). In addition, a disadvantage of the single parent offspring regression approach used in this study is sensitivity to assortative mating (Falconer 1989). The parasitic jaeger is one of the few species for which there is evidence for a correlation in overall body size (principal component 1 (PC1)) within mated pairs (Phillips and Furness 1997). It may be this that is partly responsible for the high heritability of chick condition, as condition may to some extent be related to chick structural size. Important fitness traits should in general show lower heritabilities than metric traits because little additive genetic variance remains in a population at equilibrium (Fisher 1930)

4 Notes 2293 or because they are subject to additional environmental noise (Price and Schluter 1991). In parasitic jaegers, timing of breeding clearly has an important bearing on chick survival until recruitment into Shetland colonies. The standard errors of our heritability estimates for this trait were wide, therefore a great deal of confidence cannot be placed in the exact value; nonetheless the results suggest that heritability is low. Nonsignificant parent offspring regressions in laying or hatching date have been recorded in several species (Newton and Marquiss 1984; Boag and van Noordwijk 1987; Perdeck and Cavé 1992; Hochachka 1993), and heritability values in others tend to be low (Newton and Marquiss 1984; Gustafsson 1986). Parasitic jaegers on Foula do therefore conform to this pattern, which is consistent with Fisher s theorem. By comparison, the high heritability of chick body condition in parasitic jaegers is surprising, given the importance of this trait to juvenile survival. Although the degree of heritability of body mass is variable among species, heritabilities of morphological traits, such as wing length, tarsus length, or bill dimensions, are frequently very high (Grant 1986; Wiggins 1989; Gebhardt-Henrich and van Noordwijk 1991; Schluter and Gustafsson 1993). This is despite an important influence of body size on survival or fecundity shown in several studies (Monaghan and Metcalfe 1986; Sedinger et al. 1995). Therefore, while apparently running counter to Fisher s theorem, the high degree of heritability of chick condition in parasitic jaegers is not at odds with the general trend for morphological traits. In addition, the results of recent studies suggest a variety of mechanisms that may act to maintain genetic variance in fitness-related traits (see Price et al. 1988; Alatalo et al. 1990). Acknowledgements We are grateful to the Holbourn family for permission to work on Foula, and thanks are extended to the many fieldworkers who helped to find and band parasitic jaeger chicks over the years. The British Trust for Ornithology kindly provided band-recovery data. Part of this research was funded by grants from the Shetland Oil Terminal Environmental Advisory Group. R.A.P. was supported by a Natural Environment Research Council Studentship. Kate Lessells, Paulo Catry, and two anonymous reviewers made helpful comments on early drafts of the manuscript. References Alatalo, R.V., Gustaffson, L., and Lundberg, A Phenotypic selection on heritable size traits: environmental variance and genetic response. Am. Nat. 135: Boag, P.T., and van Noordwijk, A.J Quantitative genetics. In Avian genetics: a population and ecological approach. Edited by F.A. Cooke and P.A. Buckley. Academic Press, London. pp Bolton, M Food delivery to nestling storm petrels: limitation or regulation? Funct. Ecol. 9: Cooke, F., Rockwell, R.F., and Lank, D.B The snow geese of La Pérouse Bay: natural selection in the wild. Oxford University Press, Oxford. Falconer, D.S Introduction to quantitative genetics. 3rd ed. Longman, London. Fisher, R.A The genetical theory of natural selection. Dover, New York. Gebhardt-Henrich, S.G., and van Noordwijk, A.J Nestling growth in the great tit 1. Heritability estimates under different environmental conditions. J. Evol. Biol. 3: Grant, P.R Ecology and evolution of Darwin s finches. Princeton University Press, Princeton, N.J. Gustafsson, L Lifetime reproductive success and heritability: empirical support for Fisher s fundamental theorem. Am. Nat. 128: Hakkarainen, H., Korpimäki, E., Ryssy, J., and Vikström, S Low heritability in morphological characters of Tengmalm s owls: the role of cyclic food and laying date? Evol. Ecol. 10: Hochachka, W.M Repeatable reproduction in song sparrows. Auk, 110: Monaghan, P., and Metcalfe, N.B On being the right size: natural selection and body size in the herring gull. Evolution, 40: Newton, I., and Marquiss, M Seasonal trend in the breeding performance of sparrowhawks. J. Anim. Ecol. 53: Nisbet, I.C.T., and Drury, W.H Post-fledging survival in herring gulls in relation to brood-size and date of hatching. Bird-banding, 43: O Donald, P The Arctic skua: a study of the ecology and evolution of a seabird. Cambridge University Press, Cambridge. Perdeck, A.C., and Cavé, A.J Laying date in the coot: effects of age and mate choice. J. Anim. Ecol. 61: Perrins, C.M., Harris, M.P., and Britton, C.K Survival of Manx shearwaters Puffinus puffinus. Ibis, 115: Phillips, R.A Population ecology of Arctic skuas Stercorarius parasiticus on Foula, Ph.D. thesis, University of Glasgow, Glasgow, U.K. Phillips, R.A., and Furness, R.W Predicting the sex of parasitic jaegers by discriminant analysis. Colon. Waterbirds, 20: Phillips, R.A., and Furness, R.W Repeatability of breeding parameters in Arctic skuas. J. Avian Biol. 29: Phillips, R.A., Caldow, R.W.G., and Furness, R.W The influence of food availability on the breeding effort and reproductive success of Arctic skuas Stercorarius parasiticus. Ibis, 138: Potti, J Environmental, ontogenetic, and genetic variation in egg size of Pied Flycatchers. Can. J. Zool. 71: Price, T.D., and Schluter, D On the low heritability of lifehistory traits. Evolution, 45: Price, T.D., Kirkpatrick, M., and Arnold, S.J Directional selection and the evolution of breeding date in birds. Science (Washington, D.C.), 240: Schluter, D., and Gustafsson, L Maternal inheritance of condition and clutch size in the collared flycatcher. Evolution, 47: Sedinger, J.S., Flint, P.L., and Lindberg, M.S Environmental influence on life-history traits: growth, survival, and fecundity in black brant (Branta bernicla). Ecology, 76: Spear, L., and Nur, N Brood size, hatching order and hatching date: effects on four life-history stages from hatching to recruitment in western gulls. J. Anim. Ecol. 63: van Noordwijk, A.J Quantitative ecological genetics of great tits. In Avian genetics: a population and ecological ap-

5 2294 Can. J. Zool. Vol. 76, 1998 proach. Edited by F.A. Cooke and P.A. Buckley. Academic Press, London. pp van Noordwijk, A.J., van Balen, J.H., and Scharloo, W Heritability of ecologically important traits in the great tit. Ardea, 68: Wiggins, D.A Heritability of body size in cross-fostered tree swallow broods. Evolution, 43: Wiggins, D.A Natural selection on body size and laying date in the tree swallow. Evolution, 45:

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