Local genetic structure in red grouse (Lagopus lagopus scoticus): evidence from microsatellite DNA markers

Allelic variation at seven hypervariable tri- and tetranucleotide microsatellite loci was used to determine levels of population differentiation between 14 populations of red grouse ( Lagopus lagopus scoticus ) in northeast Scotland, UK. Despite the potential for long-distance dispersal in grouse, and a semicontinuous habitat, significant population divergence was observed (mean R _ST = 0.153; P < 0.01) and an isolation-by-distance effect detected (Mantel test: P < 0.001). Examination of the spatial trend in principal component scores derived from allele frequencies among populations highlighted a barrier to gene flow that was confounding a simple isolation-by-distance effect. This barrier corresponded to an area of unsuitable habitat for grouse associated with a river system that bisected the study area. Mean genetic relatedness was higher for males than for females in all but one of the study populations, suggesting that the territorial behaviour and natal philopatry displayed by cocks have a manifold effect in generating the observed spatial genetic structure. Lower female relatedness values suggest a higher level of female-mediated gene flow, which is sufficient to prevent the loss of genetic variation from within populations and the onset of inbreeding effects. The potential consequences of local subdivision for red grouse populations are discussed.     

Temporal changes in kin structure through a population cycle in a territorial bird, the red grouse Lagopus lagopus scoticus

Populations of red grouse ( Lagopus lagopus scoticus ) undergo regular multiannual cycles in abundance. The 'kinship hypothesis' posits that such cycles are caused by changes in kin structure among territorial males producing delayed density-dependent changes in aggressiveness, which in turn influence recruitment and regulate density. The kinship hypothesis makes several specific predictions about the levels of kinship, aggressiveness and recruitment through a population cycle: (i) kin structure will build up during the increase phase of a cycle, but break down prior to peak density; (ii) kin structure influences aggressiveness, such that there will be a negative relationship between kinship and aggressiveness over the years; (iii) as aggressiveness regulates recruitment and density, there will be a negative relationship between aggressiveness in one year and both recruitment and density in the next; (iv) as kin structure influences recruitment via an affect on aggressiveness, there will be a positive relationship between kinship in one year and recruitment the next. Here we test these predictions through the course of an 8-year cycle in a natural population of red grouse in northeast Scotland, using microsatellite DNA markers to resolve changing patterns of kin structure, and supra-orbital comb height of grouse as an index of aggressiveness. Both kin structure and aggressiveness were dynamic through the course of the cycle, and changing patterns were entirely consistent with the expectations of the kinship hypothesis. Results are discussed in relation to potential drivers of population regulation and implications of dynamic kin structure for population genetics.     

General properties of predictive population models in red grouse (Lagopus lagopus scoticus)

Summary The general properties of an empirical predictive model of population fluctuations in red grouse are discussed. The model incorporates two observed time-lagged relationships between (a) chick production and spring numbers two years earlier, and (b) overwinter survival and numbers in spring one year earlier. The model produced oscillations which were slowly damped with a period of nine years. The addition of randomly-imposed poor breeding sustained the amplitude of oscillations but did not affect the period. Incorporating immigration at low densities reduced the amplitude but preserved the period. Cycle length varied with the model parameters but was generally between 8–10 years. A model with reduced lags of one and zero years could produce shorter cycles of 4–6 years.     

Parasites reduce territorial behaviour in red grouse (Lagopus lagopus scoticus)

Hypotheses for the cause of population cycles have focused on the role of intrinsic mechanisms such as spacing behaviour and extrinsic mechanisms such as parasitism and predation. This paper examines the interaction between the two dominant hypotheses in the cycles of red grouse, parasitism and spacing behaviour. The influence of the caecal nematode, Trichostrongylus tenuis, on male aggressiveness was investigated using two approaches. First, the territorial behaviour of a group of male grouse experimentally treated with an anthelmintic to reduce parasite intensities was compared with a control group with natural intensities of infection. Second, the response of treated and control males to a novel conspecific territorial intruder were recorded using playback tests. Treated males, with reduced levels of parasitism, won significantly more territorial contests than control males and produced more aggressive behaviour in response to the playback recordings. These results show that parasite removal enhanced aggressive behaviour. Implications of these results on red grouse population dynamics are discussed.     

The pervalence of caecal threadworms (Trichostrongylus tenuis) in red grouse (Lagopus lagopus scoticus)

Summary Ninety percent of wild red grouse examined carried threadworms in their intenstinal caeca. Old birds had 30 times as many worms as young birds. Some infections were as high as 30,000 worms. The occurrence of worms in old grouse conformed to the negative binomial distribution.     

Faecal egg counts provide a reliable measure of Trichostrongylus tenuis intensities in free-living red grouse Lagopus lagopus scoticus

The reliability of different egg counting methods for estimating the intensity of Trichostrongylus tenuis infections in red grouse, Lagopus lagopus scoticus, was investigated in the autumn, when grouse may harbour high parasite intensities. Possible limitations to the use of these methods were also examined. Faecal egg counts were found to accurately estimate T. tenuis worm intensities, at least up to an observed maximum of c. 8000 worms. Two egg counting methods (smear and McMaster) gave consistent results, although the exact relationship with worm intensity differed according to the method used. Faecal egg counts significantly decreased with increasing length of sample storage time, but egg counts were reliable for estimating worm intensity for three weeks. The concentration of eggs in the caecum was also found to reliably estimate worm intensity. However, egg counts from frozen gut samples cannot be used to estimate worm intensities. These results conclude that, despite some limitations, faecal and caecum egg counts provide useful and reliable ways of measuring T. tenuis intensities in red grouse.     

Philopatry, kin clusters, and genetic relatedness in a population of woodrats (Neotoma macrotis)

Studies of highly kin-structured mammal societies have revealedthe importance of natal philopatry in determining the distributionof genetic variation within populations. In comparison, therelationship between philopatry and genetic diversity withinpopulations of moderately kin-structured societies has receivedrelatively little attention. Previous studies of Neotoma macrotishave suggested that females form distinct kin clusters. Eachkin cluster overlaps spatially with the home range(s) of oneor more males that are not related to each other or to the femaleswith which they are spatially associated. To examine interactionsbetween philopatry and genetic structure in this apparentlymoderately kin-structured species, we characterized spatialand genetic relationships among individually marked femalesin a population of N. macrotis from central coastal California.Our field studies revealed that, contrary to expectation, femalesin this population were not strongly philopatric and spatiallyclustered females were not characterized by high levels of geneticrelatedness. Nevertheless, genetic structure was evident withinthe study population; spatial and genetic distances among femaleswere significantly correlated, suggesting that dispersal patternsinfluenced genetic structure even in the absence of marked femalephilopatry. Because females with overlapping spatial distributionswere not typically closely related to one another, opportunitiesfor the evolution of kin-selected social behavior (e.g., cooperativecare of young) appear to be limited in this population.     

Spatial genetic relationships in a population of the Japanese wood mouse Apodemus argenteus

Space-related relationships between individuals were investigated during the breeding season in a natural population of Apodemus argenteus (Temminck) by using the catch-mark-release method and microsatellite DNA markers. Several overlapping patterns of home ranges in breeding males and females were observed. Although this species is thought to be monogamous, DNA analysis revealed polygynous mating. In adults, relatedness between sexes was generally low and no apparent spatial genetic structure was observed. In juveniles, however, relatedness and geographical distance be-tween individuals were significantly negatively correlated. The relatedness between adult females decreased with distance, whereas there was not such a correlation in males. Long-distance movements were observed in current-year-born males. The differences in spatial genetic structure between adults and juveniles are thought to be produced by male-biased natal dispersal. An erratum to this article can be found at     

Fine-scale genetic structuring in a natural population of European wild rabbits (Oryctolagus cuniculus)

The genetic structure of a free-living tagged population of European wild rabbits (Oryctolagus cuniculus) was investigated for two consecutive years (1990 and 1991) using 10 polymorphic microsatellite loci. A specific social behaviour, the formation of stable breeding groups, influenced the genetic structure of the population. These breeding groups were shown to constitute genetically differentiated units with low levels of gene flow between them. The average relatedness among members of a social group was higher than within the population as a whole. As a result of female philopatry coupled with male-biased natal dispersal, the relatedness of females was higher than that of males, both within social groups and in the whole population. Furthermore, the average relatedness of females within groups was twice the relatedness of females between groups. This study reveals marked fine-scale, intrapopulation genetic structure, which is attributable to the social behaviour of the European wild rabbit.     

Individual and social discounting in a viscous population

Social discounting in economics involves applying a diminishing weight to community-wide benefits or costs into the future. It impacts on public policy decisions involving future positive or negative effects, but there is no consensus on the correct basis for determining the social discount rate. This study presents an evolutionary biological framework for social discounting. How an organism should value future benefits to its local community is governed by the extent to which members of the community in the future are likely to be its kin. Trade-offs between immediate and delayed benefits to an individual or to its community are analysed for a modelled patch-structured iteroparous population with limited dispersal. It is shown that the social discount rate is generally lower than the individual (private) discount rate. The difference in the two rates is most pronounced, in ratio terms, when the dispersal level is low and the hazard rate for patch destruction is much smaller than the individual mortality rate. When decisions involve enforced collective action rather than individuals acting independently, social investment increases but the social discount rate remains the same.     

Families in space: relatedness in the Barents Sea population of polar bears (Ursus maritimus)

The kin structure and dispersal pattern of polar bears ( Ursus maritimus ) of the Barents Sea was investigated during the spring mating season using two complementary approaches. First, individual genotypes based on the analyses of 27 microsatellite loci of 583 polar bears were related to field information gathered from 1146 bears in order to reconstruct the animals' pedigrees and to infer geographical distances between adult bears of different relatedness categories. According to the data, the median natal dispersal distance of the male animals was 52 km while that of the females was 93 km. Second, the relatedness of pairs of adult bears was estimated and correlated to the geographical distance between them. The female dyads had a much stronger kin structure than the male dyads. The 'pedigree approach' revealed a male kin structure which could not be detected using the 'relatedness approach'. This suggests that, on a broader scale, effective dispersal is slightly male biased. Despite fidelity to natal areas, male-mediated gene flow may nevertheless prevent genetic differentiation. Males might occasionally shift their home range which could therefore lead to a male-biased breeding dispersal. Our results showed that a nonterritorial species such as the polar bear that has a high dispersal potential, lives in a highly unstable environment and migrates seasonally is still able to exhibit a distinct kin structure during the mating season.     

From population structure to individual behaviour: genetic analysis of social structure in the European wild rabbit (Oryctolagus cuniculus)

The European wild rabbit (Oryctolagus cuniculus) lives in stable, territorial breeding groups, with male-biased natal dispersal, female philopatry, and a polygynous mating system. It was introduced into Britain in the 11 th century and kept in captive warrens as a food and fur resource. Populations expanded in the wild in the 18th century. Microsatellite markers were employed to examine the genetic structure of wild rabbit populations on three spatial scales: macrogeographic structure of 17 populations in East Anglia, microgeographic structure of a tagged population in the grounds of the University of East Anglia over four consecutive years, and pairwise kinships and individual movement within this tagged population. Populations across East Anglia were found to be genetically distinct, and heterozygote deficits were observed at all loci indicating sub-division within sampled populations. Analysis of the tagged population confirmed that rabbit populations are genetically sub-divided among social groups. Studying this population over four consecutive years revealed that as the population size increased, the number of social groups increased. Analysis of individual pairwise relatedness of females indicated that individuals did not necessarily group with kin, and behavioural data indicate that an optimum group size may exist which maximizes reproductive success.     

Host-parasite kinship in a female-philopatric bird population: evidence from relatedness trend analysis

Conspecific brood parasitism (CBP), an alternative reproductive tactic where some females lay eggs in the nests of other females of the same species, occurs in many animals with egg care. It is particularly common in waterfowl, for reasons that are debated. Many waterfowl females nest near their birthplace, making it likely that some local females are relatives. We analyse brood parasitism in a Hudson Bay population of common eiders, testing predictions from two alternative hypotheses on the role of relatedness in CBP. Some models predict host-parasite relatedness, others predict that parasites avoid close relatives as hosts. To distinguish between the alternatives, we use a novel approach, where the relatedness of host-parasite pairs is tested against the spatial population trend in pairwise relatedness. We estimate parasitism, nest take-over and relatedness with protein fingerprinting and bandsharing analysis of egg albumen, nondestructively sampled from each new egg in the nest throughout the laying period. The results refute the hypothesis that parasites avoid laying eggs in the nests of related hosts, and corroborate the alternative of host-parasite relatedness. With an estimated r of 0.12-0.14, females laying eggs in the same nest are on average closer kin than nesting neighbour females. Absence of a population trend in female pairwise relatedness vs. distance implies that host-parasite relatedness is not only an effect of strong natal philopatry: some additional form of kin bias is also involved.     

Population genetic structure of the common warthog (Phacochoerus africanus) in Uganda: evidence for a strong philopatry among warthogs and social structure breakdown in a disturbed population

Fine‐scale genetic structure of large mammals is rarely analysed. Yet it is potentially important in estimating gene flow between the now fragmented wildlife habitats and in predicting re‐colonization following local extinction events. In this study, we examined the extent to which warthog populations from five localities in Uganda are genetically structured using both mitochondrial control region sequence and microsatellite allele length variation. Four of the localities (Queen Elizabeth, Murchison Falls, Lake Mburo and Kidepo Valley) are national parks with relatively good wildlife protection practices and the other (Luwero), not a protected area, is characterized by a great deal of hunting. In the total sample, significant genetic differentiation was observed at both the mtDNA locus (F_ST = 0.68; P < 0.001) and the microsatellite loci (F_ST = 0.14; P < 0.001). Despite the relatively short geographical distances between populations, significant genetic differentiation was observed in all pair‐wise population comparisons at the two marker sets (mtDNA F_ST = 0.21–0.79, P < 0.001; microsatellite F_ST = 0.074–0.191, P < 0.001). Significant heterozygote deficiency was observed at most loci within protected areas while no significant deviation from Hardy–Weinberg expectation was observed in the unprotected Luwero population. We explain these results in terms of: (i) a strong philopatry among warthogs, (ii) a Wahlund effect resulting from the sampling regime and (iii) break down of social structure in the disturbed Luwero population.     

Investigating the loss of recruitment potential in red grouse (Lagopus lagopus scoticus): the relative importance of hen mortality,food supply,tick infestation and louping-ill

Ticks and their pathogens cause significant disease and economic loss in many animal populations. Despite this, experiments that test the impact of ticks and tick-borne diseases on wild animal populations are rare. Here, we report on an experiment assessing the effect of ticks on red grouse productivity and chick growth in relation to other causes of poor recruitment at two sites in the Scottish uplands during 2005. Treated hens received two leg bands impregnated with the acaricide permethrin, while controls hens were untreated. Chicks were captured at c.2 weeks of age and fitted with a metal patagial tag, and chicks from treated hens also received a permethrin-impregnated strip. Mean tick burdens in treated chicks were close to zero compared with a mean of around 12 in the control group. Although treatment reduced tick infestations, it did not increase brood size. Growth rates in chicks from control and treated hens were similar during the first 10 days and comparable with chicks fed an ad-lib invertebrate-based diet. These results suggest that in this case, neither ticks (and the tick transmitted louping-ill virus) nor food shortages was the main cause of chick mortality. However, mortality in the adult hens was around 35 %, and predation accounted for 62 % of these losses before broods fledged. Our results indicate that on our study sites, predation may have a more important impact on grouse population dynamics than ticks and tick-borne disease. We suggest that it may be more cost effective to determine the causes of poor grouse population performance before implementing popular but expensive tick control measures such as the culling of alternative hosts and running acaracide treated sheep ‘tick-mop’ flocks.