Rapidly declining fine-scale spatial genetic structure in female red deer

A growing literature now documents the presence of fine-scale genetic structure in wild vertebrate populations. Breeding population size, levels of dispersal and polygyny--all hypothesized to affect population genetic structure--are known to be influenced by ecological conditions experienced by populations. However the possibility of temporal or spatial variation in fine-scale genetic structure as a result of ecological change is rarely considered or explored. Here we investigate temporal variation in fine-scale genetic structure in a red deer population on the Isle or Rum, Scotland. We document extremely fine-scale spatial genetic structure (< 100 m) amongst females but not males across a 24-year study period during which resource competition has intensified and the population has reached habitat carrying capacity. Based on census data, adult deer were allocated to one of three subpopulations in each year of the study. Global F(ST) estimates for females generated using these subpopulations decreased over the study period, indicating a rapid decline in fine-scale genetic structure of the population. Global F(ST) estimates for males were not different from zero across the study period. Using census and genetic data, we illustrate that, as a consequence of a release from culling early in the study period, the number of breeding females has increased while levels of polygyny have decreased in this population. We found little evidence for increasing dispersal between subpopulations over time in either sex. We argue that both increasing female population size and decreasing polygyny could explain the decline in female population genetic structure.     

The genetic architecture of maternal effects across ontogeny in the red deer

Maternal effects, either environmental or genetic in origin, are an underappreciated source of phenotypic variance in natural populations. Maternal genetic effects have the potential to constrain or enhance the evolution of offspring traits depending on their magnitude and their genetic correlation with direct genetic effects. We estimated the maternal effect variance and its genetic component for 12 traits expressed over the life history in a pedigreed population of wild red deer (morphology, survival/longevity, breeding success). We only found support for maternal genetic effect variance in the two neonatal morphological traits: birth weight ( = 0.31) and birth leg length ( = 0.17). For these two traits, the genetic correlation between maternal and direct additive effects was not significantly different from zero, indicating no constraint to evolution from genetic architecture. In contrast, variance in maternal genetic effects enhanced the additive genetic variance available to respond to natural selection. Maternal effect variance was negligible for late-life traits. We found no evidence for sex differences in either the direct or maternal genetic architecture of offspring traits. Our results suggest that maternal genetic effect variance declines over the lifetime, but also that this additional heritable genetic variation may facilitate evolutionary responses of early-life traits.     

Sex-specific strategies of dentine depletion in red deer

Worn teeth in herbivore ungulates may be related to lower efficiency in mastication and hence lower performance. However, selection should favour maximal performance in terms of body mass and reproductive capacity during reproductive lifespan, when permanent teeth are already partially worn. We hypothesize that wear rate may respond to a strategy of use of tooth materials (notably dentine), which balances instantaneous wear rate and performance against tooth preservation for future performance and reproduction. In the present study, we investigated 4151 carcasses of Iberian red deer Cervus elaphus hispanicus and show that more worn molars were not related to lower performance throughout age. By comparing between sexes, tooth wear rates were smaller in females than in males, but the relationship between tooth wear and body performance also differed between the sexes: females did not show a significant relationship between tooth wear and performance but males with more worn teeth were in general heavier and had larger antlers until senile age, when more depleted teeth were related to smaller antlers. These results reveal, for the first time, sex-specific lifetime strategies of dentine expenditure: maintenance of performance ability throughout a longer reproductive lifespan in females, compared with maximizing current performance by depleting dentine reserves within a shorter lifespan in males.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 487–497.     

Polygyny can increase rather than decrease genetic diversity contributed by males relative to females: evidence from red deer

Polygyny is expected to erode genetic variability by reducing the diversity of genetic contribution of males to the next generation, although empirical evidence shows that genetic variability in polygynous populations is not lost as rapidly as expected. We used microsatellite markers to study the genetic variability transmitted by mothers and fathers to offspring during a reproductive season in wild populations of a polygynous mammal, the red deer. Contrary to expectations, we found that males contributed more genetic diversity than females. Also, we compared study populations with different degrees of polygyny to find that polygyny was not related to a decrease in genetic diversity contributed by males. On the contrary, when population genetic diversity was relatively low, polygyny associated with higher genetic diversity of paternal lineage. Our results show that sexual selection, by favouring heterozygote individuals, may compensate the potential reduction of effective population size caused by polygyny, thus contributing to explain why genetic diversity is not depleted in polygynous systems.     

Antler size in red deer: heritability and selection but no evolution

We present estimates of the selection on and the heritability of a male secondary sexual weapon in a wild population: antler size in red deer. Male red deer with large antlers had increased lifetime breeding success, both before and after correcting for body size, generating a standardized selection gradient of 0.44 (+/- 0.18 SE). Despite substantial age- and environment-related variation, antler size was also heritable (heritability of antler mass = 0.33 +/- 0.12). However the observed selection did not generate an evolutionary response in antler size over the study period of nearly 30 years, and there was no evidence of a positive genetic correlation between antler size and fitness nor of a positive association between breeding values for antler size and fitness. Our results are consistent with the hypothesis that a heritable trait under directional selection will not evolve if associations between the measured trait and fitness are determined by environmental covariances: In red deer males, for example, both antler size and success in the fights for mates may be heavily dependent on an individual's nutritional state.     

Age-specific feeding cessation in male red deer during rut

Tactics for resource-use involve both using stored reserves (capital breeding) and feeding while reproducing (income breeding). In polygynous ungulates, males often use an income breeding strategy when young and shift to a capital breeding tactic at prime age. Little is known regarding why prime-aged males stop or largely reduce eating during rut but still remain inactive for as much time as before rut. A detailed exploration of how rumen content correlates with age and date may shed light on the ultimate causes of why some males stop eating. We provide quantitative empirical data on rumen content from red deer Cervus elaphus during the rutting season in Norway. In male red deer, rumen content declined with age, up to around 6 years of age. Above this age, rumen content was low and stable. A time-of-year effect on rumen content was best described with a second-order polynomial term, as rumen fill was lowest during mid-October when the mass loss of males and the ovulation rate of females both peak. We present two new hypotheses related to why males reduce eating ( physical rest and parasite hypotheses). Two related patterns need to be explained and better documented: (1) why are resting times stable before, after and during rut, and (2) why do non-prime-aged males eat more between rutting activities?     

Variable extent of hybridization between invasive sika (Cervus nippon) and native red deer (C. elaphus) in a small geographical area

Instances of hybridization between endemic and alien species pose a threat to species integrity but also provide us with an opportunity to study the dynamics of gene flow between two species as they first meet. Here, we used variation at 22 highly differentiated microsatellite loci and one mitochondrial DNA (mtDNA) marker in a sample of 735 individuals, to investigate the genetic consequences of an introduction of Japanese sika deer ( Cervus nippon ) for native red deer ( C. elaphus ) on the Kintyre Peninsula in Scotland. We investigated population structure, estimated null-allele frequency and assigned individual hybrid scores using a Bayesian clustering algorithm implemented in structure 2.2. The dataset clearly divided into two clusters and generally, introgression into red and sika was low. However at one site, West Loch Awe, 43% of individuals were hybrids. MtDNA introgression indicated that hybridization was occurring between red-deer hinds and sika-deer stags. We argue that the pattern of differential introgression across the study area is primarily due to the rarity of hybridization events between the two species and the limited time the two species have been in contact (< 120 years). This contrasts with the causes of classic mosaic hybrid zones (selection induced by habitat variability). Currently, it seems possible that, in time, the level of hybridization found at West Loch Awe could also be found across the whole of the peninsula.     

Hypodermosis in the red deer Cervus elaphus in Cordoba, Spain

The prevalence of red deer hypodermosis and the life cycle of Hypodermia diana Brauer 1858 in three provinces of the south of Spain, Córdoba, Jaen and Ciudad Real, were studied by inspecting 254, thirty-eight and thirty-five deer from each province respectively. The prevalence of infestations was: Córdoba, 87.75%; Jaen, 92.10%, Ciudad Real, 91.42%. From this we deduced an overall prevalence of 88.67%, comprising 88.23% in male deer and 89.96% in female deer. The intensity of the parasitism in 213 of the 245 animals from Córdoba varied between one warble per animal to more than 100 in 28 of the inspected animals. The chronology of the life cycle during the hunting period (October to the end of February) was investigated.     

Estimating selection on neonatal traits in red deer using elasticity path analysis

Van Tienderen recently published a method that links selection gradients between a phenotypic trait and multiple fitness components with the effects of these fitness components on the population growth rate (mean absolute fitness). The method allows selection to be simultaneously estimated across multiple fitness components in a population dynamic framework. In this paper we apply the method to a population of red deer living in the North Block of the Isle of Rum, Scotland. We show that (1) selection on birth date and birth weight can operate through multiple fitness components simultaneously; (2) our estimates of the response to selection are consistent with the observed change in trait values that we cannot explain with environmental and phenotypic covariates; (3) selection on both traits has fluctuated over the course of the study; (4) selection operates through different fitness components in different years; and (5) no environmental covariates correlate with selection because different fitness components respond to density and climatic variation in contrasting ways.     

Short- and long-term effects of winter and spring weather on growth and survival of red deer in Norway

Populations of red deer (Cervus elaphus) in Norway have increased continuously over the last decades. We tested the possible effects of climate and increase in population size on the survival rates and body condition of individuals in one of the northernmost populations of red deer in Europe. Based on 678 individuals of known age marked between 1977 and 1995, we estimated annual survival rates, the probabilities of being harvested and the recapture probability according to sex, age, year, winter and spring weather, population size, and, body weight and body condition, using capture-mark-recapture models. Winter harshness negatively influenced the body weight of yearlings and the survival of calves of both sexes. Spring weather influenced the survival of males in all age classes. A negative trend during the study period was detected in body weight and condition of calves and yearlings, but not in any age- or sex- specific survival rates. No significant gender differences in mean survival were shown in any age class. Moreover, there was little (male) or no (female) detectable between-year variation in survival rates for yearlings and adults. Winter weather acts as a limiting factor on population growth through a short-term effect on first-year survival and a long-term effect on body weight. We discuss the surprising low sex differences in natural survival rates and the differential effects of winter harshness on body weight, body condition and survival in relation to life history characteristics of red deer. Received: 10 November 1997 / Accepted: 2 June 1998     

Phylogeography of red deer (Cervus elaphus) in Europe

Aim To investigate the phylogeographical patterns of red deer (Cervus elaphus) in Europe, and to disentangle the influence of ancient (e.g. Pleistocene ice ages) from more recent processes (e.g. human translocations). Location Europe. Methods In this study we provide by far the most extensive analysis of genetic structure in European red deer, based on analyses of variation at two mitochondrial markers (cyt b and D‐loop) in a large number of individuals from 39 locations. Relationships of mitochondrial DNA haplotypes were determined using minimum spanning networks and phylogenetic analyses. Population structure was examined by analyses of molecular variance. Historical processes shaping the present patterns were inferred from nested clade analysis and nucleotide diversity statistics. Results Within Europe, we detected three deeply divergent mitochondrial DNA lineages. The three lineages displayed a phylogeographical pattern dividing individuals into western European, eastern European and Mediterranean (Sardinia, Spain and Africa) groups, suggesting contraction into three separate refugia during the last glaciation. Few haplotypes were shared among these three groups, a finding also confirmed by F_ST values. Calculations of divergence times suggest that the groups probably split during the Pleistocene. Main conclusions The observed pattern is interpreted to result from isolation in different refugia during the last glaciation. The western and eastern European lineages could be linked to an Iberian and Balkan refugium, respectively. The third lineage might originate from a Sardinian or African refugium. We link local phylogeographical patterns observed in Europe to the post‐glacial recolonization process, shaped by the geographical localization of refugia and barriers to gene flow. Regardless of the importance of red deer as a game species and the tradition of translocating red deer in Europe, we detected few individuals that did not match the trichotomous pattern, suggesting that translocations have occurred mainly at smaller spatial scales.