S41.4: Inbreeding depression and its effects on natal dispersal in wild birds

Department of Biology, Virginia Polytechnic Institute and State University, Blacksburg VA. 24061-0406, USA, fax 540 231 9307, ¹e-mail sdaniels@vt.edu; ²e-mail jrwalt@vt.edu

The relationship between inbreeding depression and natal dispersal continues to be a subject of great interest to avian biologists. Both subjects—natal dispersal and the fitness costs of inbreeding—have been notoriously difficult to study, but as long-term data accumulate, pedigrees deepen, and genetic technologies advance, some progress is being made. Evidence of inbreeding depression in wild populations is building (e.g. Bensch et al.1994; Kempenaers et al.1996; Keller 1998; Daniels and Walters in press), and local natal dispersal patterns have been analyzed with respect to kinship in some species (e.g. Negro et al.1997; Wheelwright and Mauck 1998; Daniels and Walters in press). Still, determining underlying relationships remains a great challenge. Here, we summarise recent research on the costs of close inbreeding and their effects on natal dispersal in populations of wild birds. We examine what is known about inbreeding depression, the spatial distributions of relatives and their relationship to dispersal distances, and changes in dispersal behaviour in the presence of relatives.

Two separate effects of close inbreeding on fitness have been documented in wild birds: reduced hatching rates (Bulmer 1973; Greenwood et al.1978; van Noordwijk and Scharloo 1981; Rosenfield and Bielefeldt 1992; Bensch et al.1994; Kempenaers et al.1996; Keller 1998; Daniels and Walters in press) and lowered survival (Keller 1998; Daniels and Walters in press). Reduced hatching rate has become the classic component of inbreeding depression in birds, having been shown in a range of species including the Great Tit (Parus major, Bulmer 1973; Greenwood et al.1978; van Noordwijk and Scharloo 1981), Blue Tit Parus caeruleus (Kempenaers et al.1996), Great Reed Warbler Acrocephalus arundinaceus (Bensch et al.1994), Red-cockaded Woodpecker Picoides borealis (Daniels and Walters in press), Song Sparrow Melospiza melodia (Keller 1998), and Cooper’s Hawk Accipiter cooperii (Rosenfield and Bielefeldt 1992). Hatching may also be reduced for closely related pairs of Darwin’s Medium Ground Finches Geospiza fortis: had Gibbs and Grant (1989) used one-tailed tests in their analyses, related pairs would have shown significantly lower hatching rates (Gibbs and Grant 1989, L. Gibbs pers. comm.). Although Arcese (1989) reported no effect of inbreeding on reproduction in Song Sparrows, significant effects were found as more data became available (Keller 1998). If the data of Gibbs and Grant (1989) are interpreted as evidence of reduced hatching among related pairs, then to our knowledge this component of inbreeding depression has been reported in all studies in which it was assessed.

Reduced hatching success has been reported for inbred females (Keller 1998) as well as related pairs (Bensch et al.1994; Kempenaers et al.1996; Daniels and Walters in press). In Great Tits, reduced hatching success may be compensated by increased nestling survival (van Noordwijk and Scharloo 1981), but no such compensation was found for Blue Tits (Kempenaers et al.1996), Great Reed Warblers (Bensch et al.1994), or Red-cockaded Woodpeckers (Daniels and Walters in press).

Lowered survival of inbred young has been documented less often, probably in part because it is more difficult to show, but it has been demonstrated in a few species of birds. In Red-cockaded Woodpeckers, there was a significant effect of inbreeding on survival of fledglings to age one year  (Daniels and Walters in press). In a remarkable study of inbreeding depression in Song Sparrows, Keller (1998) reported that close inbreeding (inbreeding coefficient equal to 0.25) reduced survival of Song Sparrows from egg to breeding age by 49 percent, and survival of adults by 24 percent. And, again, had Gibbs and Grant (1989) employed one-tailed tests, they would have demonstrated a marginally significant reduction in survival of inbred fledglings (inbreeding coefficient greater than 0.0), despite very low sample sizes (Gibbs and Grant 1989, L. Gibbs pers. comm.).

Effects of inbreeding on the survival of Song Sparrows were most pronounced during severe environmental conditions (Keller et al.1994; Keller 1998), and results of research in other taxa also suggest that the effects of inbreeding on survival can have a strong environmental component (Jimenez et al.1994; Miller 1994; Frankham 1996). The potential for such an interaction between environment and inbreeding makes it difficult to conclude that inbreeding has no fitness effect in a given species or population, because the environmental conditions under which an effect is expressed may not have occurred during the study period.

Given the accumulating evidence of the costs of close inbreeding in wild birds, it is reasonable to expect an effect of these costs on natal dispersal. Testing such expectations requires considerable data that may be difficult to collect, but is straightforward if the data are available. There are at least two ways in which inbreeding depression could influence natal dispersal. First, if close inbreeding is costly and close relatives are predictably distributed in space, then natal dispersal distance may have evolved in part to reduce matings with these relatives. To examine this effect one must determine the spatial distribution of relatives within a population and whether dispersal distances are sufficient to avoid close inbreeding. In this instance kin are distinguished from non-kin based on distance from the natal territory, and recognition of individual kin is not required. Second, natal dispersal behaviour may change in the presence of close relatives. This effect may be manifested in decisions about whether to disperse from the natal territory, dispersal distance, dispersal destination, or other aspects of dispersal behaviour. Here, a system of active kin recognition is required.

Whether dispersal distance has evolved in part to avoid close inbreeding remains a problematic and controversial issue. Studies of sex-biased dispersal (reviewed by Pusey 1987 and Pusey and Wolf 1996) suggest such a mechanism, but lack the detail required for conclusive evidence. Studies of inbreeding rates within populations have suggested that there may be no such mechanism (van Tierenden and van Noordwijk 1988, Gibbs and Grant 1989). These studies show no difference between observed inbreeding and expected values based on simulations of random pairing (van Tierenden and van Noordwijk 1988, Gibbs and Grant 1989, but see Daniels 1997 and Wheelwright and Mauck 1998), but because all individuals within common dispersal range are included in the null model, this null may incorporate inbreeding avoidance behaviours (Part 1996). In other words, the null model assumes random dispersal, and random dispersal within a population may itself be, according to Part (1996), an efficient inbreeding avoidance mechanism. Again, more specific documentation of where relatives are and how far individual birds disperse is needed to understand the relationship between dispersal distance and inbreeding.

In a recent and noteworthy study, Wheelwright and Mauck (1998) examined philopatry, natal dispersal, and inbreeding in an island population of migratory Savannah Sparrows Passerculus sandwichensis based on nine years of data. Fledglings in their study area were strikingly philopatric: roughly 70 percent of new breeders were known to have fledged within or adjacent to the 7.6 ha. study area. Natal dispersal distances for these new breeders, within the study area, were farther than expected based on simulations of random dispersal from the natal site to any yearling nest. There were no instances of close inbreeding within the study period, a rate significantly lower than expected from simulations of random pairing of all individuals attempting to nest. However, these results do not constitute conclusive evidence that the observed natal dispersal distances represent an adaptation to avoid inbreeding depression. Dispersal distance was not sex-biased, it was not shown to be sufficient to avoid relatives as mates, and, according to the authors, there was ample opportunity for inbreeding within the study area. Also, no estimate of the costs of close inbreeding was possible because no data were available. This study did show that dispersal behaviour changes in the presence of kin (see below).

We examined the spatial distribution of kin and natal dispersal distance of females in the cooperatively breeding Red-cockaded Woodpecker, using sixteen years of data from over 200 breeding groups—virtually all the groups within a 110,000 ha. study area (Daniels and Walters in press). First, we documented significant costs of close inbreeding (see above). Next, by mapping the location of relatives, we showed that closely related males are not randomly distributed throughout the population; rather, they are clustered near a female’s natal territory. In our study, no closely related male was found farther than three territories from the female’s natal site. Surprisingly, however, females do not disperse far enough to avoid these relatives as mates; most females dispersed only one or two territories. Mean, median, and modal natal dispersal distances for females were 2.8, 2, and 1 territories respectively. Although closely related males were clustered near the natal territory, they were present at fairly low frequencies: l0 percent or fewer of the breeding males on territories within two kilometres of a breeding female were close relatives (excluding the natal site). We concluded, therefore, that despite significant costs of close inbreeding and a highly predictable distribution of kin, once a female disperses from her natal territory the distance that she moves is not affected by the relatively low risk of inbreeding. Females dispersing distances far enough to avoid any risk of inbreeding may suffer a survival cost from longer dispersal, or a reduced probability of obtaining a breeding position.

Arcese (1989) found no evidence that dispersal distance of Song Sparrows served to avoid relatives as potential mates. For birds in this population, the number of territories dispersed was unrelated to the probability of settling with a relative (Arcese 1989). Similarly, van Tierenden and van Noordwijk (1988) reported an even distribution of relatives of opposite sex across a distance gradient within a small population of Great Tits, and concluded that dispersal within this population was not influenced by the costs of inbreeding. In these species the distribution of relatives is not predictable enough with distance that they can be avoided, unless an individual leaves the population entirely.

At present, therefore, we lack conclusive evidence that dispersal distance alone, in the absence of another active kin recognition system, serves to avoid related mates and the costs of close inbreeding in any avian species. It seems unlikely that inbreeding avoidance is a primary determinant of dispersal distance in birds. This does not mean that dispersal and dispersal distance are unaffected by inbreeding depression. We now look for an effect elsewhere, in changing dispersal behaviour in the presence of kin.

Classic examples of inbreeding avoidance through changing behaviour in the presence of kin are the reproductive inhibition exhibited by Acorn Woodpeckers Melanerpes formicivorus (Koenig and Pitelka 1979) and the breeding dispersal of many co-operative breeders (Koenig et al.1984; Woolfenden and Fitzpatrick 1984; Rabenold 1985; Walters et al.1988). Here, though, we are concerned with change in natal dispersal behaviour when relatives are present.

One aspect of natal dispersal that may change in the presence of relatives is the frequency of dispersal from the natal site. In Red-cockaded Woodpeckers, females remain on their natal territories significantly more often than expected if there is no closely related breeding male present in the year following fledging (Daniels and Walters in press). Thus, natal dispersal in this species is clearly influenced by the costs of close inbreeding.

Other ways in which dispersal behaviour may change when relatives are present on the natal territory are an increase in dispersal distance and/or a change in destination. The presence of a parent of the opposite sex was not related to natal dispersal distance of Savannah Sparrows (Wheelwright and Mauck 1998) or Indigo Buntings Passerina cyanea (Payne 1991). Savannah Sparrows did change destinations if parents were present, however: one year-old breeders were more than twice as likely to nest in a different field than their natal one if a parent of the opposite sex was present on the natal site (Wheelwright and Mauck 1998). If only a parent of the same sex was present, dispersal destination was not affected (Wheelwright and Mauck 1998). This study also examined the effect of familiar and unfamiliar siblings on natal dispersal. Nests of familiar siblings were separated by greater distances than expected, and nests of unfamiliar siblings were separated by shorter distances than expected based on simulations of random dispersal within the study area (Wheelwright and Mauck 1998). These results strongly suggest that the presence of familiar relatives affects the natal dispersal of Savannah Sparrows in this island population.

Natal dispersal distance of Red-cockaded Woodpeckers was not affected by the presence of relatives near, but not on, the natal territory (Daniels and Walters in press). Female Red-cockaded Woodpeckers did not increase dispersal distances in the presence of closely related males in the neighborhood of the natal territory. Additionally, the frequency with which the nearest vacancy was occupied was unaffected by the presence of a closely related male in that territory. Our study, however, did not distinguish between familiar and unfamiliar relatives.

Evidence of the costs of close inbreeding in wild birds is growing. Reduced hatching rates are common, and lowered survival occurs in at least some species. In addition, inbreeding effects can be influenced by environmental conditions. Despite the prohibitive amount of data required to document an effect of inbreeding depression on natal dispersal, costs of close inbreeding have been shown to affect dispersal behaviours in at least two species: the likelihood of dispersal of female Red-cockaded Woodpeckers from the natal site changes in the presence of closely related males, and the destination of dispersing Savannah Sparrows changes in the presence of opposite-sex parents on the natal site.

While evidence of effects of inbreeding costs on natal dispersal could be viewed as minimal, conclusive evidence of the absence of such effects is also sparse. In the colonially breeding Lesser Kestrel Falco naumanni, the frequency of dispersal to another colony was not related to whether or not a parent of the opposite sex was present in the natal colony (Negro et al.1997). Natal dispersal distance of Indigo Buntings did not change with the presence of an opposite-sex parent, dispersal distance of Song Sparrows was not correlated with the probability of settling with a relative, and relatives were evenly distributed throughout a small population of Great Tits. Several of these studies considered kinship effects on only one aspect of natal dispersal. We do not expect that dispersal is affected by inbreeding costs in all species, but we recommend that several behaviours be analyzed before one concludes that these costs have no influence on the dispersal of a particular species. Responses to the presence of a close relative appear more widespread than general effects on dispersal distance.

Certainly other factors besides inbreeding depression affect dispersal behaviour. For example, the benefits of philopatry appear to be overwhelmingly important in determining natal dispersal patterns in some species (e.g. Negro et al.1997; Wheelwright and Mauck 1998). Interestingly though, it is in highly philopatric species such as the Savannah Sparrow and the Red-cockaded Woodpecker that local dispersal may be most strongly influenced by inbreeding depression, simply because the likelihood of inbreeding in these species is magnified.

Benefits of philopatry are not well documented, but the theory for understanding these benefits is well-developed (Greenwood 1987; reviewed by Wheelwright and Mauck 1998). Such benefits may include familiarity with the local area (the ecological model; Hinde 1956; Bengtsson 1978; Greenwood 1980), retention of local adaptations (the ecogenetic model; Templeton et al.1986; Greenwood 1987), and retention of co-adapted gene complexes (the genetic model; Shields 1982; Templeton et al.1986). In the Red-cockaded Woodpecker, extremely short dispersal distances are probably not maintained by local adaptation or co-adaptation because moderately related mates are found at equal proportions within and beyond the distance most females disperse (Daniels and Walters in press). Breeding vacancies for this species are severely constrained by a single critical resource (Walters et al.1988), and so familiarity with breeding opportunities may drive dispersal distance by conferring a competitive advantage to nearby individuals (Walters et al.1988; Daniels and Walters in press). Processes in other species may be very different; research into why some species are highly philopatric is sorely needed, but may take some time to complete considering that even the degree of philopatry remains unknown for most species.

Natal dispersal behaviour is likely a trade-off between the costs of dispersal and the costs of philopatry (Bengtsson 1978), or viewed in another way, dispersal may be a compromise between the benefits of dispersal and the benefits of philopatry. One of the documented costs of philopatry in many (perhaps even most) species is inbreeding depression. In species in which the benefits of philopatry are high, local dispersal behaviour may change through recognition of individual kin so that inbreeding costs are avoided. Recognition of kin is probably accomplished through familiarity (i.e. association, Holmes and Sherman 1983; Wheelwright and Mauck 1998), although more than a single mechanism may be in place (Daniels and Walters in press) and mechanisms may vary among species. No evidence exists, at this time, that local dispersal distances of philopatric species serve to avoid close inbreeding without the active recognition of kin. Familiar kin on the natal territory clearly are avoided as mates in several species, and familiar kin on other territories may be. There is no evidence that unfamiliar kin on other territories are avoided. Perhaps other behavioural mechanisms might be involved in avoiding inbreeding depression, e.g., divorce might be a mechanism to rearrange pairs after a first unsuccessful breeding attempt and thereby reduce inbreeding. In Red-cockaded Woodpeckers, as in many avian species, new pairs that fail are especially likely to divorce (Daniels 1997). However, Kempenaers et al. (in press) showed that the number of unhatched eggs is not related to tendency to divorce.

Much more research in all these areas—costs and benefits of dispersal, degree and ecological basis of philopatry, and kin recognition systems—is necessary before the relationships between inbreeding and natal dispersal can be determined. The necessary evidence will most likely come from long-term studies of marked populations.

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