Polymorphism and transcription of Mhc class I genes in a passerine bird, the great reed warbler

 The class I genes of the major histocompatibility complex (Mhc) are here investigated for the first time in a passerine bird. The great reed warbler is a rare species in Sweden with a few semi-isolated populations. Yet, we found extensive Mhc class I variation in the study population. The variable exon 3, corresponding to the α₂ domain, was amplified from genomic DNA with degenerated primers. Seven different genomic class I sequences were detected in a single individual. One of the sequences had a deletion leading to a shift in the reading frame, indicating that it was not a functional gene. A randomly selected clone was used as a probe for restriction fragment length polymorphism (RFLP) studies in combination with the restriction enzyme Pvu II. The RFLP pattern was complex with 21–25 RFLP fragments per individual and extensive variation. Forty-nine RFLP genotypes were detected in 55 tested individuals. To study the number of transcribed genes, we isolated 14 Mhc class I clones from a cDNA library from a single individual. We found eight different sequences of four different lengths (1.3–2.2 kilobases), suggesting there are at least four transcribed loci. The number of nonsynonymous substitutions (d _N ) in the peptide binding region of exon 3 were higher than the number of synonymous substitutions (d _S ), indicating balancing selection in this region. The number of transcribed genes and the numerous RFLP fragments found so far suggest that the great reed warbler does not have a "minimal essential Mhc" as has been suggested for the chicken. Received: 13 May 1998 / Revised: 18 August 1998     

No evidence for inbreeding avoidance in a great reed warbler population

Inbreeding depression may drive the evolution of inbreedingavoidance through dispersal and mate choice. In birds, manyspecies show female-biased dispersal, which is an effectiveinbreeding avoidance mechanism. In contrast, there is scarceevidence in birds for kin discriminative mate choice, whichmay, at least partly, reflect difficulties detecting it. First,kin discrimination may be realized as dispersal, and this isdifficult to distinguish from other causes of dispersal. Second,even within small, isolated populations, it is often difficultto determine the potential candidates available to a femalewhen choosing a mate. We sought evidence for inbreeding avoidancevia kin discrimination in a breeding population of great reedwarblers (Acrocephalus arundinaceus) studied over 17 years.Inbreeding depression is strong in the population, suggestingthat it would be adaptive to avoid relatives as mates. Detaileddata on timing of settlement and mate search movements madeit possible to identify candidate mates for each female, andlong-term pedigrees and resolved parentage enabled us to estimaterelatedness between females and their candidate mates. We foundno evidence for kin discrimination: mate choice was random withrespect to relatedness when all mate-choice events were considered,and, after correction for multiple tests, also in all breedingyears. We suggest that dispersal is a sufficient inbreedingavoidance mechanism in most situations, although the lack ofkin discriminative mate choice has negative consequences forsome females, because they end up mating with closely relatedmales that lowers their fitness.     

Low frequency of extrapair paternity in the polygynous great reed warbler, Acrocephalus arundinaceus

We carried out DNA fingerprinting on 553 young (130 broods)great reed warblers (Acrocephalus arundnaceus) in 1987–1991.In the study population, where 40% of the males become polygynous,there was a low frequency of extrapair fertilizations (EPF).When data from all five years were pooled, 3.1% of the youngwere sired by extrapair males (EPF-males) and 5.4% of the broodscontained extrapair young. We found no cases of extrapair maternity;young with 6–17 mismatched DNA bands (n= 17) had highband sharing with their putative mothers (range = 0.52–0.72)but low band sharing with their putative fathers (range = 0.24–0.40).In broods exposed to EPF, on average 53% of the young were siredby EPF-males. We found the genetic father to each of the illegitimateyoung. In all cases the same EPF-male sired all extrapair youngin a brood. Broods containing EPF-young tended to be initiatedlate during the breeding season. Breeding attempts were ratherevenly distributed over two months, thus this breeding asynchronywould have facilitated EPFs. There was no difference in EPFfrequency between broods where the pair males had left theirfemales unguarded during parts of their fertile periods andbroods where males guarded throughout the fertile periods. Nestswith extrapair young had significantly shorter mean distanceto the closest male neighbor and more male neighbors within100 m than nests without extrapair young. We found no indicationthat females engaged in EPF to get parental care from the EPF-males,or because they were forced to copulate with extrapair males.The low frequency of EPF suggested that females did not seekgenetic diversity to their brood. We cannot rule out the possibilitythat females engaged in EPF to insure fertility. However, datasupporting this hypothesis were weak. Instead, our data supportthe conclusion that females engaged in EPF to increase the geneticquality of their offspring, and that females may have used malesong repertoire size as a cue when choosing EPF partners.     

An analysis of hatching success in the great reed warbler Acrocephalus arundinaceus

Hatching success is a potentially important fitness component for avian species. Previous studies of hatching success in natural populations have primarily focused on effects of inbreeding but a general understanding of variation in hatching success is lacking. We analyse data on hatching success in a population of great reed warblers Acrocephalus arundinaceus in Lake Kvismaren in south central Sweden. The effects of a range of covariates, including three measures of inbreeding as well as effects of classifications in the data (such as identities of individuals), on hatching success are analysed simultaneously. This is done by means of fitting Bayesian binomial mixed models using Markov chain Monte Carlo methods. Using random effects for each individual parent we check for unexplained variation in hatching success among male and female individuals and compare it to effects of covariates such as degree of inbreeding. Model selection showed that there was a significant amount of unexplained variation in hatching probability between females. This was manifested by a few females laying eggs with a substantially lower hatching success than the majority of the females. The deviations were of the same order of magnitude as the significant effect of parent relatedness on hatching success. Whereas the negative effect of parent relatedness on hatchability is an expression of inbreeding, the female individual effect is not due to inbreeding and could reflect maternal effects, that females differ in fertilisation and/or incubation ability, or an over representation of genetic components from the female acting on the early developing embryo.     

Establishment and maintenance of the breeding territory in the polygynous great reed warbler

Settlement of male great reed warblers in the breeding ground was highly asynchronous at Lake Biwa in Japan. It took over 1 month from the appearance of the first male to a saturation in number of males. In resource-defense-polygyny, males are expected to try to defend as large an area as possible in the optimal habitat. In fact, a small number of the earliest settling males divided up the breeding ground almost completely as territories among themselves and these were later reduced in size with the addition of later settlers. The reduction was not due to a seasonal decline of aggressiveness on the part of the owners but to a higher level of intrusion pressure by later arriving males. The neighbor-neighbor relationship, once established, was rather stable. Home range overlap was small and territorial contacts were few between neighbors. Territorial boundaries seem not to shift despite the addition of new males as long as the neighbors were the same. The stable relationships between neighbors are expected to help the earlier resident to maintain his large and good territories throughout the breeding season and hence polygyny is favored in this species.     

Restricted dispersal reduces the strength of spatial density dependence in a tropical bird population

Spatial processes could play an important role in density-dependent population regulation because the disproportionate use of poor quality habitats as population size increases is widespread in animal populations-the so-called buffer effect. While the buffer effect patterns and their demographic consequences have been described in a number of wild populations, much less is known about how dispersal affects distribution patterns and ultimately density dependence. Here, we investigated the role of dispersal in spatial density dependence using an extraordinarily detailed dataset from a reintroduced Mauritius kestrel (Falco punctatus) population with a territorial (despotic) breeding system. We show that recruitment rates varied significantly between territories, and that territory occupancy was related to its recruitment rate, both of which are consistent with the buffer effect theory. However, we also show that restricted dispersal affects the patterns of territory occupancy with the territories close to release sites being occupied sooner and for longer as the population has grown than the territories further away. As a result of these dispersal patterns, the strength of spatial density dependence is significantly reduced. We conclude that restricted dispersal can modify spatial density dependence in the wild, which has implications for the way population dynamics are likely to be impacted by environmental change.     

Dynamics of parasitemia of malaria parasites in a naturally and experimentally infected migratory songbird, the great reed warbler Acrocephalus arundinaceus

Little is known about the development of infection of malaria parasites of the genus Plasmodium in wild birds. We used qPCR, targeting specific mitochondrial lineages of Plasmodium ashfordi (GRW2) and Plasmodium relictum (GRW4), to monitor changes in intensities of parasitemia in captive great reed warblers Acrocephalus arundinaceus from summer to spring. The study involved both naturally infected adults and experimentally infected juveniles. The experiment demonstrated that P. ashfordi and P. relictum lineages differ substantially in several life-history traits (e.g. prepatent period and dynamics of parasitemia) and that individual hosts show substantial differences in responses to these infections. The intensity of parasitemia of lineages in mixed infections co-varied positively, suggesting a control mechanism by the host that is general across the parasite lineages. The intensity of parasitemia for individual hosts was highly repeatable suggesting variation between the host individuals in their genetic or acquired control of the infections. In future studies, care must be taken to avoid mixed infections in wild caught donors, and when possible use mosquitoes for the experiments as inoculation of infectious blood ignores important initial stages of the contact between the bird and the parasite.     

Repertoire size, sexual selection, and offspring viability in the great reed warbler: changing patterns in space and time

Only a few studies have focussed on the consistency of sexualselection patterns in space and time. One such case is the greatreed warbler (Acrocephalus arundinaceus), for which studiesin Germany in 1981–1982 and Sweden in 1987–1991strongly suggested that the size of a male's song repertoirewas the target of mate choice and sexual selection. Studyingthe same German population once again in 1994–2000, weinvestigated the consistency of these patterns over time aswell as between populations. Our reanalysis of the data from1981–1982 shows that male repertoire size was positivelycorrelated with male pairing success (harem size) and with clutchsize (adjusted for seasonal effects), whereas no such correlationswere found during 1994–2000 in the same population. Wesuggest that the earlier correlations were probably caused indirectlyby covariation with territory quality, and that a decline inpopulation size has changed the role of territory quality. Inthe Swedish population, an earlier study found a striking correlationbetween the size of a male's repertoire and the viability ofits offspring, suggesting good-gene effects. In contrast, wefound no such correlation in the German population, neitherin 1981–1982 nor in 1994–2000. We conclude thatrepertoire size does not seem to be a very reliable indicatorof variation in male quality. Interestingly, the analysis ofdata from 1994–2000 showed that male pairing success wasstrongly correlated with measures of strophe length and immediateversatility, traits that have been found to reflect male longevity.Future studies will have to show whether these performance-relatedtraits are more powerful indicators of male quality than isrepertoire size.     

Phenological differences among selected residents and long-distance migrant bird species in central Europe

The phenological responses to climate of residents and migrants (short- and long-distance) differ. Although few previous studies have focussed on this topic, the agree that changes in phenology are more apparent for residents than for long-distance migrants. We analysed the breeding times of two selected residents (Sitta europaea, Parus major) and one long-distance migrant (Ficedula albicollis) from 1961 to 2007 in central Europe. The timing of the phenophases of all three bird species showed a significant advance to earlier times. Nevertheless, the most marked shift was observed for the long-distance migrant (1.9 days per decade on average in mean laying date with linearity at the 99.9 % confidence level). In contrast, the shifts shown by the residents were smaller (1.6 days for S. europaea and 1.5 days for P. major also on average in mean laying date for both, with linearity at the 95 % confidence level). Spearman rank correlation coefficients calculated for pairs of phenophases of given bird species in 20-year subsamples (e.g. 1961–1980, 1962–1981) showed higher phenological separation between the residents and the migrant. This separation is most apparent after the 1980s. Thus, our results indicate that the interconnections between the studied phenological stages of the three bird species are becoming weaker.     

Seed dispersal in a patchy environment with global age dependence

A model of seed population dynamics proposed by S. A. Levin, A. Hastings, and D. Cohen is presented and analyzed. With the environment considered as a mosaic of patches, patch age is used along with time as an independent variable. Local dynamics depend not only on the local state, but also on the global environment via dispersal modelled by an integral over all patch ages. Basic technical properties of the time varying solutions are examined; necessary and sufficient conditions for nontrivial steady states are given; and general sufficient conditions for global asymptotic stability of these steady states are established. Primary tools of analysis include a hybrid Picard iteration, fixed point methods, monotonicity of solution structure, and upper and lower solutions for differential equations.This work was supported in part by National Science Foundation Grants MCS-7903497 and MCS-790349701     

Corticosterone,food intake and refueling in a long-distance migrant

Elevated baseline corticosterone levels function to mobilize energy in predictable life-history stages, such as bird migration. At the same time, baseline corticosterone has a permissive effect on the accumulation of fat stores (fueling) needed for migratory flight. Most migrants alternate flight bouts with stopovers, during which they replenish the fuel used during the preceding flight (refueling). The role of corticosterone in refueling is currently unclear. In a fasting–re-feeding experiment on northern wheatears (Oenanthe oenanthe) in autumn we found that baseline total and free corticosterone levels were negatively related with both food intake and the rate of fuel deposition after fasting. This confirms our earlier findings in wild conspecifics in spring and indicates that corticosterone does not stimulate stopover refueling. Whether the negative relationship between baseline corticosterone level and fuel deposition rate is causal is questionable, because within-individual comparison of corticosterone metabolite levels in droppings did not reveal differences between refueling and control periods. In other words, corticosterone does not appear to be down-regulated during refueling, which would be expected if it directly hampers refueling. We discuss possible correlates of corticosterone level that may explain the negative association between corticosterone and stopover refueling. Additionally, we found that fasting decreases total corticosterone level, which contrasts with previous studies. We propose that the difference is due to the other studies being conducted outside of the migration life-history stage, and provide a possible explanation for the decrease in corticosterone during fasting in migrating birds.     

Digestive tract function in the long-distance migratory garden warbler,Sylvia borin

Digestive tract morphology and function of captive garden warblers (Sylvia borin) were measured during four stages of their endogenous circannual rhythm: before, during and after their autumn fattening prior to migration to wintering grounds in Africa, and after a partially simulated migratory flight. Food intake increased by 33% during fattening, utilization efficiency of dry matter tended to increase, and that of energy increased significantly (P0.01). This was because digestive tract capacity (measured as dry tissue mass) increased, so that mean retention time of food remained constant before, during and after fattening (80–84 min). After a 48-h period of starvation of fattened birds to partially simulate a migratory flight, food intake was lower on the first day of refeeding than on the next 4 days, and utilization efficiency was higher on that day, at least partly because of a longer mean retention time (111 min versus 78 min on the third day). Digestive tract dry tissue mass fell by 50% during starvation, and that of the small intestine by 63%. It is concluded that the garden warbler adapts to long-distance migration without feeding by rapidly reducing the size of its digestive tract, an expensive tissue to maintain, during migration in order to save weight and energy, and possibly also to supply part of the fuel and protein required for the flight. The cost of this strategy appears to be the time taken to rebuild the gut at stopover sites with food, but the low probability of finding such a site in the Sahara Desert means that this strategy is probably optimal for garden warblers.     

Avian seed dispersal and seedling distribution of the endangered tree species,Taxus chinensis,in patchy habitats

Background: There is limited understanding about bird dispersal behaviour and seedling distribution of endangered tree species in patchy environments, although these processes are important for plant species persistence.

Aims: We tested how patch features affected bird behaviour and seed dispersal, and thus seedling distribution of the endangered Chinese yew tree (Taxus chinensis).

Methods: In the present study, we combined field data of bird dispersal behaviour and GIS-based information to elucidate the influence of spatial features of habitat patches on bird dispersal behaviour, and the resulting effects on the seedling distribution of the endangered Chinese yew in two patchy habitats.

Results: Our results showed that the only seed source patch could attract eight bird species for dispersal at the two sites. Post-foraging movements of bird dispersers was strongly related to both topography and the relative locations of habitat patches. Yew seedlings aggregated only at the seed source and bamboo recruitment patches, which was affect by both the spatial distribution of recruitment patches and patch use by dispersers.

Conclusions: Our results emphasise that bamboo patches in both patchy environments provide the necessary conditions for germination of yew seeds, and the post-foraging behaviour of dispersers determines seed deposited in these patches. Our study highlights the importance of the dispersal behaviour of frugivorous birds in the successful regeneration and colonisation of yew populations in patchy habitats.     

Philopatry analysis of the great reed warbler (Acrocephalus arundinaceus) based on ringing data in Europe

Ringing databases of the EURING Data Bank and the Hungarian Bird Ringing Centre were analysed in order to investigate the philopatry of the great reed warbler (Acrocephalus arundinaceus) in three European regions. The aim of the study was to find out if there are continent-scale geographic trends in philopatry with respect to the age of the birds. Three clusters were assigned according to their geographic positions: (i) southern part of Europe (Region 1: between 36°–43° latitudes), (ii) middle part of Europe (Region 2: between 43°–49° latitudes) and (iii) northern part of Europe, (Region 3: between 49°–56° latitudes). No significant differences were found between the natal and breeding philopatry in any Regions, except Region 3. The birds ringed as adults in Region 3 were less faithful to their breeding site than those of the other two regions. Natal philopatry of juveniles did not differ between Region 1 and Region 2, but both of them differed in this respect from Region 3. A method for choosing appropriate breeding periods in philopatry studies is also proposed.     

Within‐ and between‐season repeatability of eggshell colouration in the great reed warbler Acrocephalus arundinaceus

While avian eggshell colouration has attracted biologists for decades, little is known about its variation within individuals. The main goal of this study was to explore within‐ and between‐season repeatability of eggshell appearance in the great reed warbler Acrocephalus arundinaceus. To achieve this, we measured eggshell reflectance of first and replacement clutches of individual females within one breeding season, and the reflectance of their first clutches in two following breeding seasons. As environmental conditions may affect egg colouration, repeatability was estimated from linear mixed‐effects models where we initially included temperature and rainfall during egg laying, as well as year, clutch order and egg‐laying date as fixed effects, and clutch identity nested in females as random effects. Eggshell appearance within clutches showed moderate repeatability, while both within‐ and between‐season repeatability in clutch colouration for individual females was low. Our findings indicate that low intra‐clutch variation may have a function within the context of brood parasitism, i.e. in facilitating host recognition of alien eggs. With variable eggs between successive clutches, however, host females may need to relearn the appearance of their eggs with every clutch they lay. This could represent a significant constraint for host egg‐discrimination abilities. Yet, whether environmental or intrinsic physiological factors are responsible for the variation in eggshell colouration between successive clutches of the same females still remain to be discovered.     

Parent presence, delayed dispersal, and territory acquisition in the Seychelles warbler

The presence of parents in the natal territory may play an important,but often overlooked, role in natal dispersal and the consequentacquisition of a territory. Living with parents in a territorymay confer a fitness advantage to subordinates through, forexample, the nepotistic behavior of the parents or indirectbenefits gained by helping to raise nondescendent kin. Whena parent is replaced by a stepparent, such advantages are reducedor disappear and, as a result, subordinates may disperse. Subordinatesthat disperse after parent replacement may be constrained intheir timing of dispersal, which could have negative fitnessconsequences. In the cooperatively breeding Seychelles warbler,we show that when a parent was naturally replaced or experimentallyremoved and subsequently replaced by a stepparent from outsidethe territory, subordinates were more likely to disperse thanwhen both parents remained in the natal territory. Furthermore,subordinates dispersing from territories in which one or bothparents had been replaced were less likely to acquire a breederposition than subordinates dispersing when both parents werestill on the natal territory. Our findings suggest that thepresence of parents in the natal territory may promote delayeddispersal and facilitate the eventual acquisition of a breederposition outside the natal territory. Our results support theidea that the prolonged parental care, which long-lived speciesare able to provide, may have selected for family living.