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Lifetime reproductive success (LRS) of an individual is defined as the number of recruits to the following generation that the individual produces over its entire lifespan (Clutton-Brock 1988; Newton 1989a). A general pattern is that the distribution of LRS is often very skewed (see reviews in Clutton-Brock 1988; Newton 1989a). This means that most breeding individuals do not succeed in producing a recruit. As a consequence, only a small proportion of the breeding population contribute to future generations. Because LRS in natural populations is generally assumed to be a relatively good estimate of fitness (Grafen 1988; Newton 1989b; but see Benton & Grant 2000), identifying phenotypic characteristics of those successful individuals will provide important insight into the evolutionary processes in the population.
Basically, LRS consists of two components (Barrowclough & Rockwell 1993). One is the average number of recruits an individual produces in each of its years as an adult. The second is the number of reproductive seasons which is, of course, related closely to the adult life expectancy. Thus, a long adult lifespan and high annual reproductive success can both contribute to a high LRS. In general, life expectancy is an important determinant of LRS in birds (Gustafsson 1986; Newton 1989a; Grant & Grant 2000; Merilä & Sheldon 2000; Krüger & Lindström 2001) as well as in other taxa (Clutton-Brock 1988; Wauters & Dhondt 1995; Bérubé, Festa-Bianchet & Jorgenson 1999; Kruuk et al. 2000). However, the relative contribution of individual variation in adult survival rate to differences in LRS seems to differ among species. For instance, in splendid fairy-wren (Malurus splendens) lifespan accounted for 44 and 66% of the variation in male and female LRS, respectively (Rowley & Russel 1989). On the other hand, lifespan accounted for only about 5% of the variation in male and female LRS in red-billed gulls (Larus novaehollandiae scopulinus) (Mills 1989). This suggests that we must understand how a character affects survival as well as reproductive success to understand fully its effects on LRS.
A number of studies has demonstrated that a significant proportion of the variation in LRS can be related to variation in individual characteristics such as body size [Le Boeuf & Reiter 1988, in male northern elephant seals (Mirounga angustirostris); Clutton-Brock, Albon & Guinness 1988; Kruuk et al. 2000; Kruuk et al. 2002, in male and female red deer (Cervus elaphus)], body condition or body mass (Ribble 1992, in both sexes of the monogamous rodent Peromuscus californicus), or the expression of sexually selected traits [Kruuk et al. 2002, in male red deer; West & Packer 2002, in male lions (Panthera leo)]. Similarly, in birds it has also been shown that variation in LRS was related to body size [Grant & Grant 2000, in both sexes of Darwin's finches (Geospiza fortis and G. scandens); Bryant 1988, 1989, in male house martins (Delichon urbica)], plumage morph [Krüger & Lindström 2001, in both sexes of common buzzard (Buteo buteo)], as well as sexually selected traits [Hasselquist 1998, song repertoire in male great reed warblers (Acrocephalus arundinaceus); Gustafsson, Qvarnström & Sheldon 1995, size of the white forehead patch in male collared flycatchers (Ficedula albicollis)].
Several studies have indicated large intra- and interspecific sexual differences in the distribution of LRS. Such variation may be related to, for example, different degrees of polygamy (Orians & Beletsky 1989; Weatherhead & Boag 1997). However, if the level of polygamy is low, and survival equal in males and females, the variance in LRS of both sexes is expected to be similar (Newton 1989b) as found in, for example, pied flycatchers (F. hypoleuca) (Sternberg 1989).
Trivers & Willard (1973) suggested that when males have higher variance in LRS than females, it would pay for high-quality individuals to produce a high-quality son in preference to producing a high-quality daughter, because a high-quality son gives higher fitness returns. In contrast, poor-quality individuals should produce more daughters. Such differential investment in sons and daughters may occur both before and after birth (e.g. Maynard Smith 1980; Hewison & Gaillard 1999). Accordingly, there are indications that males of a number of animal species need a higher amount of resources to survive or grow (Clutton-Brock, Albon & Guinness 1985; Griffiths 1992). As an alternative to the theory of Trivers & Willard (1973), high-quality individuals are expected to produce more surviving sons because their average level of provisioning is higher (Clutton-Brock 1991), and not as a consequence of differential investment in sons and daughters per se among high- and poor-quality individuals. Both theories predict that individual quality should be related positively to number of sons they produce, but the second theory also predicts a positive relationship with number of daughters.
It has generally been quite difficult to measure LRS in natural populations. First, long-term studies are often required to follow a sufficient number of individuals throughout their lives (Newton 1989a). Secondly, having recorded the lifespan of a sufficient number of individuals, it is often difficult to measure the number of recruits an individual contributes to the population, both because it may be difficult to determine parentage of recruits (Newton 1989a) and because young individuals may emigrate and recruit into populations outside the study area (Clarke, Sæther & Røskaft 1997; Lambrechts et al. 1999). In our study metapopulation of house sparrows (Passer domesticus L.) off the coast of northern Norway these problems are negligible, because a large proportion of all individuals on the study islands have been individually marked (Ringsby et al. 1999) and genotyped. Thus, we could identify the genetic parents of recruits through DNA analyses (Ringsby et al. 1999; Jensen et al. 2003). Moreover, the main study islands were surrounded by an archipelago of 13 other islands where a considerable proportion of the house sparrows had also been individually banded. Consequently, both birds that recruited on their natal island and birds that emigrated from one of the main study islands before recruitment had a high probability of being recorded (see also Altwegg, Ringsby & Sæther 2000).
The purpose of the present study was to examine the following questions.
How is the individual variation in LRS of the two sexes related to differences in annual reproductive success and life expectancy?
Does variation in LRS relate to morphological characteristics of males and females?
Do morphological characteristics of males and females affect lifetime production of sons and daughters differently?
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This study demonstrates that lifetime reproductive success (LRS) in male and female house sparrows is affected mainly by variation in individual annual reproductive success, and to a lesser extent variation in individual lifespan (Table 2). A significant proportion of the variance in the LRS of house sparrows (Fig. 1) was explained by variation in phenotypic traits in males (Table 3, Fig. 4). Furthermore, we found that the effect of male morphology on LRS operated mainly through an effect on the number of recruited daughters (Table 3). In contrast, overall LRS of females was independent of their phenotypic characteristics, although the number of recruiting daughters was affected by female morphology (Table 3). The effect of morphology on lifespan and annual reproductive success appeared to differ in males and females, but these differences were not significant.
The importance of variation in annual reproductive success for variation in LRS is in accordance with studies on other passerines (van Balen, van Noordwijk & Visser 1987; McCleery & Perrins 1988, 1989; Gustafsson 1989; Merilä & Sheldon 2000). On the other hand, in studies where estimates of LRS are based on fledgling production instead of the production of recruits, adult lifespan often emerges as the most important component of variation in LRS (Bryant 1989; Dhondt 1989; Grant & Grant 2000). This is generally because those estimates do not account for the large variation in reproductive success that is due to variation in the probability of survival from fledging to recruitment (see Newton 1989a). Previous studies of our house sparrow metapopulation have documented large temporal variation in the survival rate of juveniles, closely related to variation in climate (Ringsby et al. 1999, 2002). Thus, it seems likely that variation in juvenile survival rate is one important reason why variation in annual reproductive success, and not lifespan of adults, is the major component of LRS in house sparrows in northern Norway. Similar effects of juvenile survival on variation in annual reproductive success, and consequently on LRS have also been documented in, for example, great tits (Parus major) (van Balen et al. 1987; McCleery & Perrins 1988, 1989) and in red deer (Clutton-Brock et al. 1988). Estimates of LRS based on the number of fledglings and not on recruits, may therefore not reflect the true relative importance of lifespan and annual reproductive success for the contribution of an individual to future generations (i.e. its fitness) (Grafen 1988).
Very few studies exploring factors related to LRS include dispersing recruits in the estimates of individual LRS (Lambrechts et al. 1999). This may result in considerable biases in estimates of LRS because some dispersal is the rule rather than the exception in most animals (Stacey, Johnson & Taper 1997). Because theories predict that either high- or low-quality individuals should disperse (Clobert et al. 2001), not including dispersing recruits may preclude detection of any effects of, for instance, morphological characteristics of parents on the LRS. In contrast, in our study we included recruits that dispersed in the estimates of LRS because the main study islands were surrounded by an archipelago of 13 islands covering an area of more than 1600 km2 where house sparrows were also captured and observed. In addition, we searched for emigrants from our study area several 10 km along the coastline on the mainland (see Methods). This suggests that sexual differences in natal dispersal, as is common in many bird species (Clarke et al. 1997), cannot account for the differences in the effects of morphology on the production of male and female recruits (Table 3).
The influence of male morphological characteristics on variation in LRS (Table 3, Fig. 4) suggests that the phenotypic characteristics of the male are important determinants of the LRS, even in such a variable environment as is found at the coast of northern Norway (Ringsby et al. 2002). This corresponds with results from studies on other bird species, that have documented significant associations between body size and either annual reproductive success or lifespan in males and/or females (Bryant 1988, 1989; Johnson & Johnston 1989; Grant & Grant 2000; Krüger & Lindström 2001). In some species a major part of the variation in juvenile survival and growth, and consequently also adult morphology, may have a stochastic component that is so considerable that the link between, for example, adult body size and parental quality is weak. This may be the case in, for instance, collared flycatchers on Gotland (Gustafsson 1989; Merilä & Sheldon 2000) and great tits in England (McCleery & Perrins 1989). Nevertheless, as suggested by the results in this and some other studies (e.g. Kruuk et al. 1999; Festa-Bianchet, Jorgenson & Réale 2000; Kruuk et al. 2002), morphological characteristics of parents may reflect individual quality despite any effects of a stochastic environment on morphology.
A few other studies have focused on the relationship between characteristics of sexually selected traits and LRS (e.g. Sheldon & Ellegren 1999; Kruuk et al. 2002). Furthermore, recent reviews of the effect of sexually selected traits on survival of offspring (Møller & Alatalo 1999) and male viability (Jennions, Møller & Petrie 2001) have indicated that sexually selected traits in general are associated positively with these factors, and should thus also be significantly related to LRS. In the house sparrow, Møller (1988, 1989, 1990) demonstrated that there was a positive relationship between the size of the sexually selected black badge of males and their annual mating success. Thus, our results support Møller's findings but are in disagreement with most other studies on house sparrows, which have found either no (Veiga 1993; Kimball 1996; Cordero, Wetton & Parkin 1999; Whitekiller et al. 2000; Václav & Hoi 2002) or a negative effect of badge size on annual reproductive success (Griffith, Owens & Burke 1999a). All these studies have, however, examined the effect of male badge size only on reproductive success within a single breeding episode, and some have not taken extra-pair offspring into account (but see Cordero et al. 1999; Griffith et al. 1999a; Whitekiller et al. 2000). One possible reason for our contrasting result is the fact that our estimates of LRS are of genetic offspring (both intra- and extra-pair) averaged over all breeding episodes of a male. Consequently, we could account for the contribution of any extra-pair young to male LRS. In addition, if badge size of males on average has a small positive effect on number of recruits each breeding season, perhaps through increased frequency of extra-pair offspring or survival of offspring, such effects will be enhanced when summing the success from all breeding episodes during the entire male lifespan. This positive effect of badge size on LRS (Table 3, Fig. 4b) suggests that badge size is an indicator of male quality, and consequently that sexual selection (Andersson 1994) may operate in the house sparrow. The positive relationship between badge size and LRS suggests that the male badge either indicates indirect (i.e. genetic) benefits that promote offspring survival or direct benefits such as, for instance, enhanced fertility, high level of parental care or a good territory or nest site (Andersson 1994; Møller 1994). We cannot, however, distinguish between these two alternatives on the basis of our results. Regardless of the ultimate mechanism, our results agree with the general belief that the expression of sexually selected traits has an effect on male fitness (e.g. LRS), as documented recently in collared flycatchers (Gustafsson et al. 1995; Pärt & Qvarnström 1997; Sheldon et al. 1997), red deer (Kruuk et al. 2002) and lions (West & Packer 2002).
The positive effect of male badge size on LRS was associated with a significant positive effect on the number of recruiting daughters, whereas it did not significantly influence the number of sons (Table 3). In females, none of the morphological characters affected the number of recruiting sons (Table 3). However, bill length, body mass and body condition of females had a positive effect on number of daughters (Table 3). In accordance with studies on other passerines (Clarke et al. 1997), it has been documented previously that dispersal among female juvenile house sparrows in our study metapopulation is almost twice as high as for males (Altwegg et al. 2000). The positive association between morphological characters of adults and number of female recruits may thus result in increased production of dispersers by these birds as well.
A number of studies on both birds and mammals have documented differential production of sons and daughters (see reviews in Sheldon 1998; Hewison & Gaillard 1999). In many cases this has been attributed to mechanisms by which parents adjust the sex ratio according to the differential fitness returns implemented in production of sons and daughters (Trivers & Willard 1973), sometimes resulting in increased production of sons by good quality parents (Ellegren, Gustafsson & Sheldon 1996; Nager et al. 1999; Sheldon et al. 1999). However, such mechanisms often depend on the assumption that variance in male reproductive success is higher than for females (Trivers & Willard 1973; Frank 1990; but see also Gowaty 1993), a condition that was not fulfilled in this study (see Fig. 1). High quality males may, however, also be predicted to invest more in daughters because such investment may be selected for by female choice (e.g. Seger & Trivers 1986). Accordingly, although we currently have no knowledge of how much different parents invest in male and female offspring in house sparrows, our results seem to imply that the level of investment in daughters is related to the morphological characteristics of adults (see Table 3). However, one can speculate whether the reason for this apparent positive relationship between investment in daughters and adult morphology may be a result of equal investment in male and female offspring, but that males with a large badge and females with long bills, high body mass and good body condition are of ‘better quality’ and thus perhaps produce more fledglings with higher average survival. Furthermore, if male offspring on average have more variable survival because they need more resources during growth and development (see Cordero et al. 2000; Westneat et al. 2002), and are consequently more sensitive to environmental conditions during the juvenile period (see e.g. Clutton-Brock et al. 1985; Sheldon et al. 1998; Lindström 1999; Badyaev 2002), the observed relationship between parental quality and production of daughters may arise without the need to invoke differential allocation by parents (see also Griffiths 1992).
Our results demonstrate that the morphology of parents affect their LRS (Table 3), a measure linked closely to fitness (e.g. Grafen 1988; Newton 1989b). Such effects of morphology will have evolutionary consequences if the traits are heritable (i.e. that they have additive genetic variance that selection can act upon) (Falconer & Mackay 1996; Lynch & Walsh 1998). In a previous study of the same metapopulation we demonstrated that bill length had a heritability of around 0·55 in both sexes, and tarsus length a heritability of 0·31 in males (Jensen et al. 2003). Moreover, we estimated that the heritability of female body mass and body condition index was 0·12 and 0·18, respectively. A cross-fostering experiment by Griffith, Owens & Burke (1999b) indicated that male badge size was not heritable, but affected mainly by environmental factors (see also Veiga & Puerta 1996; Griffith 2000). Møller (1989), however, estimated that the heritability of badge size was 0·6, but his estimate was based on a very small sample of individuals raised by their natural parents. Data from our study population indicate that the heritability of badge size is low (approximately 0·3), but significant (H. Jensen, unpublished results). Consequently, the morphological characteristics of adults that are related to production of offspring (i.e. body mass and condition in females, bill length in both sexes, and tarsus length and badge size in males) may be transmitted to their offspring. Accordingly, studies of other taxa have demonstrated that traits related to LRS may be heritable. This was demonstrated, for example, for the size of the white forehead patch in collared flycatchers (Merilä & Sheldon 2000), bill length in snow petrels (Pagodroma nivea) (Barbraud 2000) and antler mass in red deer (Kruuk et al. 2002). If selection on a trait due to its relationship with LRS is not counteracted by selection on correlated traits, the traits will evolve as a result of their effect on LRS (Falconer & Mackay 1996). In our house sparrow population, selection on traits due to their association with LRS is not counteracted by negative phenotypic correlations (Table 1). However, we have demonstrated previously the existence of a strong negative genetic correlation between bill length and body condition index in females, and a strong positive genetic correlation between bill length and tarsus length in males (Jensen et al. 2003). The negative genetic correlation between bill length and body condition index in females indicates that the positive association between these traits and production of female recruits may not result in evolutionary change in any of the traits. Moreover, because male tarsus length and bill length are constrained by a positive genetic correlation, the same will be true for these two traits in males because they appear to be selected for in opposite directions (see Table 3). Similarly, badge size in males may also be constrained by genetic correlations with other traits related to LRS (H. Jensen, unpublished results).
In this study we have documented large individual variation in LRS and identified important characteristics of individuals that are most successful in reproduction over their entire adult life. These characteristics are heritable and some may evolve as response to their effect on LRS, whereas the evolution of others may be constrained by genetic correlations with other characteristics that affect LRS. Moreover, these individual characteristics generally have a positive influence on the production of female recruits, which is the dispersing sex in house sparrows and most other passerines. Our study thus suggests important consequences of individual variation in morphology not only on the distribution of the contribution that each individual has to the gene pool in the next generation, but that this variation also may affect the evolutionary processes within local populations and probably the dynamics of the whole metapopulation.