Genetic similarity between parents predicts hatching failure: nonincestuous inbreeding in the great reed warbler?
MATERIALS AND METHODS
Species, Study Area, and Field Work
The great reed warbler is a long-distance migrant bird wintering in tropical Africa. It is facultatively polygynous (Dyrcz 1977; Catchpole et al. 1985; Urano 1985); in our study population at lake Kvismaren (59 [degrees] 10[prime]N, 15 [degrees] 25[prime]E), Sweden, about 40% of the territorial males pair with more than one (2-4) female (Hasselquist and Bensch 1991). The population was rounded by two breeding pairs in 1978 (Bensch et al. 1987) and since 1983 almost all individuals ([greater than]95%), breeding adults as well as nestlings, have been ringed (Bensch and Hasselquist 1991). The great reed warblers breed in two plots 3 km apart, Fagelsjon (Marsh A) and Rysjon (Marsh B). The present study was made in 1987-1990 when the breeding population consisted of 36, 56, 64, and 54 adults, respectively. The study involved a total of 119 adult individuals because several birds bred in two or more years. Pedigrees were made up for all breeding individuals up to their great-grandparents, however no pedigree is complete. In the pedigree analysis, both parents were identified for 48 of the 119 breeding individuals and all grandparents for five individuals. Each year about 50% of the first-time breeders were unringed when arriving, and therefore they most likely had been hatched outside our study area (Bensch and Hasselquist 1991). Three immigrants to our study population were ringed as nestlings at lake Hjalmaren, 15 km away, which is the nearest breeding site outside Kvismaren.
In this study, most nests (95%) were located during the nest-building period and inspected for the first time at the latest when we expected that it contained four eggs (day 4). All nests were inspected again at day 6 or 7 whereafter we visited the nests approximately every 5-7 d. All nests were checked at day 16 or 17 to establish hatching day and then again 2-3 d later, Eggs that were still present when the youngest nestling was at least 3 d old were registered as eggs that failed to hatch. The number of fledged young was checked on day 9 after hatching. In statistical tests, the proportions of hatched eggs in each clutch were arcsine transformed to improve normality (Sokal and Rohlf 1981). To meet criteria for independence, we used the average values for combinations of males and females breeding together more than once. Significance levels are two-tailed.
In 1987-1990, we successfully collected blood samples from more than 95% of adults and young in the population together involving 104 complete families. Blood samples of 20-60 [[micro]liter], obtained by tarsus vein puncturing, were suspended in 500 [[micro]liter] of SET-buffer (0.15 M NaCl, 0.05 M TRIS, 0.001 M EDTA) and stored in a -20 [degrees] C freezer. The DNA was extracted by adding 10 [[micro]liter] of SDS (20%) and 13 [[micro]liter] of Proteinase K (10 mg/mL) and incubated overnight at 55 [degrees] C. DNA was purified by extractions with phenol, phenol/chloroform-isoamylalcohol, and chloroform-isoamylalcohol. The dissolved DNA was precipitated with 0.1 vols 3 M sodium acetate and 2 vols absolute ethanol, washed with 75% ethanol and vacuum dried whereafter the whole procedure was repeated. Eventually the DNA pellet was solved and stored in 50 [[micro]liter] TE.
We revealed true paternity of young by conducting DNA fingerprinting on 104 clutches (455 young). About 10 [[micro]gram] of total cellular DNA was digested with 18-20 units of Alu I for at least 3 h in 37 [degrees] C and subsequently electrophoresed through a 25 cm long 0.8% agarose gel in 0.5 x TBE buffer. The gels were run at 26 V for c. 70 h and then stained with ethidiumbromide and checked for the position of lambda-DNA fragments (digested by HindIII) making sure that fragments smaller than 2.0 kb had electrophoresed off the gel. To increase the transferring of long bands, the gels were soaked in 0.25 M HCI for 20 min. The DNA was transferred to nylon filters by a vacuum blot while the gels were soaked in 0.4 M NaOH. Filters were hybridized overnight at 64 [degrees] C in 5 x SSPE, 5 x Denhardt's solution, 0.5% SDS, and the radioactively labeled probe (Jeffreys' 33.15; Jeffreys et al. 1985). Filters were washed at 64 [degrees] C in 2 x SSPE and 0.1% SDS for 30 min and 2 x 30 min in 1 x SSPE and 0.1% SDS. The filters were autoradiographed for 1-7 d at -70 [degrees] C.
Bands were scored (by S.B. and D.H.) in the approximate size range of 3.0-23 kb to reveal paternity. A band was considered identical in two individuals if the distance it had migrated differed less than 0.5 mm from a band in the other individual. For each family, we assessed the proportion of band sharing [D = 2[F.sub.ab]/([F.sub.a] + [F.sub.b])] between the parents and between the mother young and father young, respectively. Parents were always run in adjacent lanes that facilitated the evaluation of band sharing. Four hundred forty-one young that showed 0-2 (394, 39, and 8) unique bands (not present in either of the putative parents) were identified as being the young of the putalive parents (see Westneat 1990), whereas 14 young with 3-7 unique bands were identified as being illegitimate.
DNA Fingerprinting and Band Sharing
Band sharing can be used to identify illegitimate young as soon as shared proportions are sufficiently different between related individuals TABULAR DATA OMITTED and between unrelated individuals. However, band sharing is a more reliable measure of overall genetic similarity if the variable number tandem repeat (VNTR) loci identified by the DNA fingerprinting technique (Jeffreys et al. 1985) are dispersed throughout the genome. This is most likely the case if the resolved alleles assort independently of each other (Jeffreys et al. 1986). Thus, before studying the effect of relatedness and genetic similarity on reproductive success we tested whether bands tended to assort independently.
For one pair of great reed warblers, we had nine young on the same autoradiogram because they raised two clutches in the same season. This made it possible to study the level of heterozygosity and linkage between loci. Out of 13 bands exclusive for the male and 14 exclusive for the female, none was transmitted to all of the nine chicks showing that the parents were heterozygous at these loci. One pair of fragments from the female and two pair of fragments from the male appeared to be alleles because they never were inherited together. From the female, one pair of fragments always occurred together, which indicated linkage. However, the transmission of pair of fragments did not indicate clumping because observed and expected numbers appeared to be similar. Here, a significance test of linkage is inappropriate because the observed distributions are generated from pairwise comparisons of nonindependent data (Wetton et al. 1987). Still, the segregation analysis shows that the majority of bands stems from alleles at different heterozygote loci, The independent assortment of the RFLP fragments in this study give merits to the usage of band sharing as an indicator of overall genetic similarity.
Based on the occurrence of at least two exclusive bands in young (Westneat 1990), we could identify five clutches (out of 104) in which at least one young had a parent different from the putative one's. Band sharing for the 14 nestlings identified as illegitimate was D = 0.30 [+ or -] 0.10 with their putative father and D = 0.56 [+ or -] 0.07 with their putative mother showing that it was the males who were the mismatched parent. In figure 2c, one young identified as being illegitimate (three unique bands) showed a high level of band sharing (D = 0.57) with the putative male suggesting that it was wrongly excluded. However, the exclusion was most certainly correct because a neighboring male that apparently had sired all the other five young in the clutch explained all diagnostic bands also in this particular chick. In fact, for all young identified as being illegitimate in this study, we found neighboring males as likely sires (EPF males) and all chicks with two to six diagnostic bands have been rerun and analyzed on a second autoradiogram confirming the results of paternity found in this analysis (Hasselquist et al. 1994). Mean band sharing ([+ or -] SD) between parents in our study was D = 0.37 [+ or -] 0.10, whereas the average band sharing between young and the true father and mother were D = 0.63 [+ or -] 0.09 and D = 0.62 [+ or -] 0.09, respectively. These figures support the hypothesis that the level of band sharing correlates with relatedness in the great reed warbler.
Figure 2a shows that there is a considerable variation in band sharing between mates; at its fight end the distribution partly overlaps that of parents and young. The comparisons include eight pairs in which the females were experimentally introduced from another distant breeding site (Bensch and Hasselquist 1992). These pairs showed significantly lower D-values ([Mathematical Expression Omitted] = 0.29 [+ or -] 0.12) than pairs in which both parents were native to the area ([Mathematical Expression Omitted] = 0.38 [+ or -] 0.10; [t.sub.90] = 2.69, P = 0.01).
Band Sharing and Reproductive Success
In the following analyses, we have excluded the eight pairs with introduced females and the five pairs involving clutches of mixed paternity. The number of fledged young was negatively correlated with the level of band sharing between parents (r = -0.33, P [is less than] 0.01, N = 80), indicating that high genetic similarity between mates entailed a fitness cost. We partitioned this fitness measure into its three components. Clutch size ([r.sub.s] = -0.08, P [is greater than] 0.1) and the survival of chicks from hatching to fledging ([r.sub.s] = -0.10, P [is greater than] 0.1) showed no relationship with parental genetical similarity, whereas proportion of hatched eggs ([r.sub.s] = -0.34, P [is less than] 0.01) was negatively correlated with the parents' D-value. The 80 pairs in this subset fledged in total 405 young of which 56 (13.8%) were later recorded as adults on breeding grounds. The proportion of fledged young becoming recruits did not correlate with the parents' D-value ([r.sub.s] = -0.07, P [is greater than] 0.1). Thus, because postfledging survival appeared to be independent of the parents D-values, a reduced fledging success caused by unhatched eggs must incur a fitness cost. Looking at the data for each year and study marsh, we found a negative correlation (r = -0.69, P [is less than] 0.05) between the average proportion of hatched eggs and the average level of band sharing. In fact, proportions of hatched eggs differed significantly between years (ANOVA, [F.sub.(3,76)] = 4.80, P = 0.004), thus we standardized the data by substracting the mean of the year from each value. Also, the level of band sharing (D) differed significantly between years (ANOVA, [F.sub.(3,76)] = 3.55, P = 0.02) and was positively correlated with the absolute number of scored bands (r = 0.45, P [is less than] 0.001). However, in a partial-correlation analysis in which we controlled for possible confounding effects of absolute number of scored bands and differences between years, band sharing still had a significant effect upon egg hatchability (partial r = -0.287, df = 76, P [is less than] 0.05). Because the residual still differed significantly from normality after the transformation of egg hatchability (Lilliefors 1967) the level of significance might be dubious. Therefore, we split the pairs in two groups. Those pairs that had at least one unhatched egg shared significantly more bands (0.43 [+ or -] 0.12) than those whose eggs all hatched (0.36 [+ or -] 0.08; t-test on arcsine-transformed band sharing proportions, [t.sub.(78)] = 2.87, P = 0.005). Thus, we conclude that parents that share many bands experience lower reproductive success because of reduced egg hatchability.
In this study, we have not evaluated whether pairs actively avoid partners with whom they would have had a high D-value. This is because we have been able to accurately assess D-values only between individuals that have been run on the most adjacent lanes on the same autoradiogram (see Piper and Rabenold 1992), in our study involving the parents and their young. However, the five clutches involving illegitimate young may suggest that females seek extra-pair copulations from males with whom they have lower D-values than with their breeding partner. In four cases, the female had lower D-values with the EPF male than with their breeding partner, whereas in one case the D-value with the EPF male was only slightly higher (0.37 versus 0.36).
During the study years (1987-1990), only a few cases of inbreeding were detected in the pedigrees. No full-sib (r = 0.5), parent and offspring (r = 0.5), half-sib (r = 0.25), or grandparent and grandoffspring (r = 0.25) matings were registered despite females having the opportunity to choose such a close kin in 12 cases (P = 0.11, exact-probability test). In this statistical test, the female's mating options were those males who actually were singing in the mating area on the day the female made her choice; for a definition of mating options see Bensch and Hasselquist (1992). In fact, the only cases of inbreeding were one pair of first cousins (r = 0.125) and one pair of full great-aunt and great-nephew (r = 0.125), which showed D-values of 0.38 and 0.39, respectively. The pair of full cousins bred together in two successive years. According to Lynch (1991), the expected D-value ([+ or -] SD) between individuals related by r = 0.125 should be D = 0.45 [+ or -] 0.10 when the average band sharing in the population is 0.37. Thus, in this study full cousins cannot by their D-values alone be separated from unrelated pairs.
On the assumption that the individuals not ringed as nestlings in the study area originate from distant populations and are not themselves inbred, we can calculate the average level of inbreeding, F, which is the average proportion of the genome that is homozygous through descent (Falconer 1981; Greenwood 1987). The F-value for this great reed warbler population is 0.0625. 3/119 = 0.0016.
Among birds, close inbreeding (r [is greater than or equal to] 0.25) affects mainly egg hatchability (Sittman et al. 1966; Greenwood et al. 1978; van Noordwijk and Scharloo 1981). Thus, our finding that the reduction in the number of fledged young because of genetic similarity between parents was caused by lower egg hatchability rather than a small clutch or low nestling survival conforms to earlier results from other species. In their study of great tits Parus major, van Noordwijk and Scharloo (1981) noted that inbred pairs suffering from reduced hatchability produced more local recruits than outbred pairs with high hatching success. They therefore concluded that there was no net cost for great tits to engage in inbreeding. Similarly, several studies have failed to find costs of inbreeding (e.g., Gibbs and Grant 1989; Hoogland 1992). In our study of great reed warblers, reduced hatching success seemed to affect fitness because pairs with high D-values did not compensate the loss of unhatched eggs by producing a higher proportion of local recruits. Remarkably, however, we failed to prove that those pairs with high level of D-values and reduced hatchability were close kins.
It can be argued that our pedigrees are incomplete and that pairs that suffer from reduced hatchability are close kin although not detected as such. This is unlikely, however, for several reasons. We have ringed almost all individuals, adults as well as nestlings, in the study area for 3 yr preceding this study as well as during the 4 study years. Because the frequency of illegitimate young is almost negligible (3%), the pedigrees observed in the years preceding this study should correspond with the true genetic pedigrees. The population is isolated, and immigrants most likely originate from several distant breeding sites and are therefore not likely to be related to each other. Also, adults are faithful to their breeding marsh in successive years (Bensch and Hasselquist 1991), and we have never recorded individuals ringed as nestlings in the study area to engage in close inbreeding. Thus, it is not likely that sibs or half sibs from other breeding sites would have dispersed to Kvismaren and there bred together. We are therefore confident to conclude that cases of close inbreeding were as rare as our field data indicated. There are at least two possible explanations why genetic similarity between nonkin mates can cause more hatching failures.
The word "inbreeding" has been used for various phenomena related to the isolation of a population and to the mating between relatives (Jacquard 1975). The level of inbreeding in a population can be measured by the coefficient of inbreeding (F), which is the probability that the two alleles at a locus in an individual are identical by descent (IBD). However, the definition of IBD is arbitrary because identity always indicates common ancestry (Maynard Smith 1989). In this study, our pedigrees cover few generations, and therefore we do not know the mating pattern of individuals some generations back. This implies that the level of inbreeding, that is, the proportion of homozygote loci relative to that in a random mating population with the same gene frequencies, can be significant because of heavy inbreeding in previous generations even though the present rate of consanguineous matings is low. In contrast to most passerine birds (e.g., Greenwood 1980) male and female great reed warblers show similar degrees of both natal and breeding dispersal (Bensch and Hasselquist 1991). Thus, in this species, differential dispersal pattern between males and females cannot act as a mechanism to avoid inbreeding (cf. Ralls et al. 1986; Hoogland 1992).
In the late 1960s, the Swedish population of great reed warblers consisted of fewer than 10 pairs (Holmbring 1973). We believe that the individuals founding our study population constituted a subsample of this population. This idea is supported by the fact that the average level of band sharing between parents in our study population (D = 0.37) is higher than those for presumably unrelated individuals of other bird species (e.g., reviewed in Reeve et al. 1990). In fact, the D-value for our great reed warbler population is almost as high as the D-values for supposedly inbred populations of the blue duck Hymenolaimus malacorhynchos (Triggs et al. 1992). Also, we found a significantly lower level of band sharing between pairs of which the female originated from a distant breeding site. Hence, repeated population bottlenecks in previous generations may have reduced the genetic variation in the present population through inbreeding (O'Brien and Evermann 1988).
If the study population suffers from a remaining inbreeding depression, one would expect the level of hatching failure to be higher in our study area than in the core area of the species distribution. The average proportion of hatching failure was 0.074 [+ or -] 0.14 eggs, a low figure compared with other bird species (Rothstein 1973) and in fact very similar to figures obtained from two East European (0.08 - 0.11, Havlin 1971; Dyrcz 1981) and one Japanese (0.05, Urano 1985) population of great reed warblers. Because egg hatchability is not lower than in other, supposedly outbred, populations this explanation requires that the individuals in our study population are more prone to avoid mating with a closely related individual than in the core population in which close inbreeding may be less costly. As mentioned before, our data did not reveal any case of close inbreeding. Also, the F-value for the great reed warbler population in this study (F = 0.0016) is in the lower range found for other species of birds [range F = 0.0011 - 0.036; (Richdale 1957; Greenwood et al. 1978; van Noordwijk and Scharloo 1981)]. Thus, whether our study population suffers from a remaining inbreeding depression, our pedigree analysis shows that the present level of inbreeding is low.
Hence, the recent history of the species distribution in Sweden, together with a comparatively high level of band sharing in the population may indicate that the study population has suffered from inbreeding depression. In an inbred population, there is an increased risk that deleterious recessive alleles come into a homozygote state also when matings occur between individuals that are "unrelated" according to pedmgree data. Thus, although the great reed warbler pairs with both a high level of band sharing and hatching failure did not appear to be relatives in our pedigrees, they might have shared many genes because they belonged to the same inbred line. According to theories of optimal inbreeding (Shields 1983), individuals should select a partner that is of intermediate genetic similarity. This optimum for the Japanese quail Coturnix japonicus has been found at the distance of cousins (r = 0.125, Bateson 1982). However, during a population bottleneck individuals may select a more distantly related individual than a cousin to keep the optimal genetic distance. Thus, inbreeding avoidance may be more adaptive in populations with reduced genetic variability. If so, a greater tendency to avoid incestuous matings can explain why the supposedly inbred population of great reed warblers at Kvismaren show an average proportion of unhatched eggs.
However, it may also be the case that our study population is not inbred in the sense outlined above. Even a moderate immigration rate from non-Swedish populations might have retarded the reduction in genetic variability (see the review about gene flow in Rockwell and Barrowclough 1987). Is it at all possible that individuals without common ancestors have such a high genetic similarity that matings between them can result in "inbreeding effects" such as hatching failure? Such negative effects of genetic similarity between mates may be of special significance at loci with an overdominance effect, for example, the polymorphic major histocompatibility complex (MHC). Interestingly, recent studies of mice show that females mate disassortatively with respect to their own set of alleles at the MHC (Ports et al. 1991). In a small population, there might be few MHC haplotypes thus limiting individuals' abilities to find a mate with a MHC that complements their own genotype. If parents sharing MHC alleles experience higher levels of abortions/hatching failure (see Potts and Wakeland 1990), we would expect to find increased levels of hatching failure at small population sizes because individuals cannot find a suitable mate that maximizes their offspring's heterozygosity at particularly important loci.
This study provides the first results showing that the degree of genetic similarity between non-kin parents, as revealed by their RFLP pattern, might have a negative effect on hatching success of eggs. Moreover, it shows that DNA fingerprinting is a powerful tool for detecting effects associated with inbreeding that is not revealed by traditional pedigree analyses. This has direct applications in conservation biology where preserving genetic diversity in small and fragmented populations often is a critical issue McCauley 1991).
For field assistance, we are most indebted to B. Nielsen, U. Ottoson, P. Frodin, F. Haas, and M. Haraldsson. We thank T. Alerstam and H. Temrin for encouragement during the initial stages of the great reed warbler study. T. Alerstam, T. Fagerstrom, M. Grahn, J. L. Hoogland, H. Kallander, and D. F. Westneat gave constructive comments on the manuscript. A. J. Jeffreys kindly provided the minisatellite probe. The field work was supported by the Elis Wide (to S.B.), J. A. Ahlstrand (to D.H.), and Hierta-Retzius Foundations (to S.B. and D.H.). The lab work was supported by grants to T.v.S. from the Swedish Natural Research Council, the Carl Trygger Foundation for Scientific Research, the Crafoord Foundation, the Carl Tesdorpf Foundation, the Maja and Erik Lindquist Research Foundation and the National Swedish Environment Protection Board. This paper is report number 74 from the Kvismare Bird Observatory.
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|Author:||Bensch, Staffan; Hasselquist, Dennis; Schantz, Torbjorn von|
|Date:||Apr 1, 1994|
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