Female-biased dispersal, low female recruitment, unpaired males, and the extinction of small and isolated bird populations

Small and isolated populations are usually assumed to be at a high risk of extinction due to environmental or demographic stochasticity, genetic problems, or too little immigration. In birds, natal dispersal is usually female-biased, but the consequences of such a pattern on vulnerability to extinction of isolated populations has not received much attention before. In this paper I derive predictions as to how female-biased natal dispersal may differentially affect the extinction risk of populations and species with contrasting distributions, migratory behaviours, life histories and mating systems. Female-biased dispersal will lead to male-biased sex ratios in small, isolated or fragmented populations, in particular because recent research has shown that females often have a limited ability to search for mates and may therefore effectively be lost from the breeding population if they disperse into areas empty of conspecifics. I reviewed published studies on birds and found that a high proportion of unpaired males is common in isolated populations or populations in small habitat fragments. Dispersal of females may therefore increase the vulnerability to extinction of small or isolated populations, or populations at the periphery of a species' distribution range. I also predict that vulnerability to extinction should be greater for migratory than for resident species and greater for short-lived than for long-lived species because of differences in the time available for females to locate unpaired males. Further, extinction risk may also be greater for birds than for mammals due to differences in which sex disperses and patterns of parental care. Finally, mating system will also affect vulnerability to extinction when natal dispersal leads to biased sex ratios. I review available evidence for these predictions (e.g. songbird declines in North America) and discuss implications for conservation.     

Drift load in populations of small size and low density

According to theory, drift load in randomly mating populations is determined by past population size, because enhanced genetic drift in small populations causes accumulation and fixation of recessive deleterious mutations of small effect. In contrast, segregating load due to mutations of low frequency should decline in smaller populations, at least when mutations are highly recessive and strongly deleterious. Strong local selection generally reduces both types of load. We tested these predictions in 13 isolated, outcrossing populations of Arabidopsis lyrata that varied in population size and plant density. Long-term size was estimated by expected heterozygosity at 20 microsatellite loci. Segregating load was assessed by comparing performance of offspring from selfings versus within-population crosses. Drift load was the heterosis effect created by interpopulation outbreeding. Results showed that segregating load was unrelated to long-term size. However, drift load was significantly higher in populations of small effective size and low density. Drift load was mostly expressed late in development, but started as early as germination and accumulated thereafter. The study largely confirms predictions of theory and illustrates that mutation accumulation can be a threat to natural populations.     

Female choice selects for lifetime lekking performance in black grouse males

''Good genes'' models assume that females can use a signal such as mating effort to assess a male''s lifetime fitness. Inferring long-term performance from short-term behavioural observations can be unreliable, and repeated sampling may be needed for more accurate assessment of males. Additionally, if sexual advertisement is viewed as a life-history trait subject to trade-offs, reliable comparison of mates should yield information on all life-history components rather than on one trait value in one season. We show that in the lekking black grouse (Tetrao tetrix), a male''s success is best explained by assuming that females are informed of the past history of males up to the beginning of the study (eight years). Much of this extremely lasting ''memory'' can be attributed to females observing long-term outcomes of male–male competition: current territory position is the only momentarily observable variable that has high power in predicting female choice, and it correlates to a male''s past lekking effort on a cumulative lifetime scale. We conclude that females can use territory position as a signal that conveys information of a male''s lifetime performance that combines lekking effort and longevity. Females may thus overcome the problem of male allocations varying in time, without the need to pay costs associated with repeated sampling.     

Offspring allocation in structured populations with dimorphic males

Summary Many fig wasp species have dimorphic males. These males often mate in different localities; one typically disperses before mating whereas the other does not disperse. In 1979 a model was developed for offspring allocation in dimorphic fig wasps, but it assumed that females only lay a single egg per fig. This assumption is not realistic and precludes any effects local mate competition (LMC) may exert on morph abundance. I develop a model without these restrictions and show that the optimal proportions of each morph is determined by two parameters. Firstly, the proportion of the non-dispersing morph is affected by the mean number of females that oviposit in a patch. This effect is due to the negative correlation between LMC between brothers and the number of females that oviposit in a patch. Secondly, the proportions of both male morphs correlate with the expected proportion of females which will mate with each morph. The separation of the two parameters generalizes the model to any other species which is spatially structured and which has two male morphs or even two alternative mating strategies. A comparison of two models shows that parent—offspring conflict involving morph ratios will not have far reaching consequences. I test these models using the 1979 model's data and both models accurately predict the variation in morph ratios in six species of dimorphic fig wasps.     

Bryozoan populations reflect nutrient enrichment and productivity gradients in rivers

1. The hypothesis that nutrient enrichment will affect bryozoan abundance was tested using two complementary investigations; a field‐based method determining bryozoan abundance in 20 rivers of different nutrient concentrations by deploying statoblast (dormant propagule) traps and an experimental laboratory microcosm study measuring bryozoan growth and mortality. These two methods confirmed independently that increased nutrient concentrations in water promote increases in the biomass of freshwater bryozoans. 2. Statoblasts of the genus Plumatella were recorded in all rivers, regardless of nutrient concentrations, demonstrating that freshwater bryozoans are widespread. Concentrations of Plumatella statoblasts were high in rivers with high nutrient concentrations relative to those with low to moderate nutrient concentrations. Regression analyses indicated that phosphorus concentrations, in particular, significantly influenced statoblast concentrations. 3. Concentrations of Lophopus crystallinus statoblasts were also higher in sites characterised by high nutrient concentrations. Logistic regression analysis revealed that the presence of L. crystallinus statoblasts was significantly associated with decreasing altitude and increasing phosphorus concentrations. This apparently rare species was found in nine rivers (out of 20), seven of which were new sites for L. crystallinus. 4. Growth rates of Fredericella sultana in laboratory microcosms increased with increasing nutrient concentration and high mortality rates were associated with low nutrient concentrations. 5. Our results indicate that bryozoans respond to increasing nutrient concentrations by increased growth, resulting in higher biomasses in enriched waters. We also found that an important component of bryozoan diets can derive from food items lacking chlorophyll a. Finally, bryozoans may be used as independent proxies for inferring trophic conditions, a feature that may be especially valuable in reconstructing historical environments by assessing the abundance of statoblasts in sediment cores.     

Components of lifetime mating success and body size in males of a scrambling damselfly

Sexual selection is hypothesized to favour small body size in males of scrambling species, that is, those in which males obtain matings by actively searching for females. I tested this hypothesis in a natural population of the scrambling emerald damselfly, Lestes sponsa. Mating efficiency (matings/visit to the pond) was the most important factor explaining variation in male lifetime mating success (LMS; 71%). This suggests a large potential for sexual selection. Path analysis of male LMS suggested a quality factor that positively affected both mating efficiency and life span. In contrast with the small-male mating advantage hypothesis, part of this potential for sexual selection was realized as stabilizing selection on male body size, indicating that there may also be a lower limit to body size for mating efficiency. This also illustrates that the constancy of body size may be explained by sexual selection alone. Survival explained about 20% of the variation in LMS and random processes were potentially important for determining LMS. My results show the problems of using mating efficiency as a measure for the intensity of sexual selection and the need to distinguish between potential and realized selection pressures, especially when comparing the importance of natural and sexual selection. I discuss mechanisms that may have caused the intermediate-male mating advantage in this scrambling species. Copyright 2000 The Association for the Study of Animal Behaviour.     

Stochastic selection in large and small populations

We describe two models of stochastic variation in selection intensity. In both models the arithmetic mean fitness of all genotypes is equal; in both models the geometric mean fitness of the heterozygous genotype is greater than that of both homozygous genotypes. In one model the correlation between the fitnesses of the homozygous genotypes is +1; in the other it is −1. We show that the expected time to absorption of an allele in a finite population is significantly retarded for all initial gene frequencies in the former model. The expected time to absorption of an allele in the latter model is retarded only at extreme initial gene frequencies; at intermediate initial gene frequencies the expected time to absorption is accelerated. We conclude that the criterion for polymorphism based on the geometric mean of the heterozygote being greater than that of both homozygotes provides only limited information about the fate of gene frequency.     

Correlations between relatives in small populations

Correlations between relatives in small, closed populations can be substantially smaller than predicted by the classical formulas of population genetics. This effect is especially pronounced for relatives whose most recent common ancestor is several generations removed. When the effective population size is small, correlations between even close relatives can be negative. This implies that in small populations conventional estimators of quantitative genetics parameters will be biased and that preferential treatment of close relatives will be less likely to evolve.     

Production efficiency in small mammal populations

Summary The data used to analyse the relationship between production (P) and respiration (R) in small mammals (Grodziski and French 1983) are reanalysed and different conclusions are drawn. Differences in production efficiency cannot be attributed to any particular trophic classe, but in the higher taxonomic categories the murids have higher production effeciency than the rest. However examination of numerous populations of the same species shows that production efficiencies of congeneric species sometimes differ significantly and show differences which exceed those between higher taxa. The same applies to trophic classes. The low slope described for the regression of P on R for Insectivora is due to an aberrant set of data for Sorex araneus. Production efficiency is directly related to litter size in rodents and inversely to survival of adults. This result conflicts with much earlier work and is discussed at length.     

Distylic Hottonia palustris shows high reproductive success in small populations despite low genetic variability

Hottonia palustris L. (Primulaceae) is characterized by a heteromorphic incompatibility system. The strategy of distylic ramets is believed to promote outcrossing, to maintain overall genetic diversity and to prevent inbreeding depression. In spite of this distyly, an extremely low amount of allozymic diversity was observed in 545 individual ramets from 14 populations in Flanders (Belgium). A possible explanation for such low genetic variation is discussed in relation to the vegetative propagating abilities and the ecological niche width of the species. In contrast to the uniformity in allozymes as well as to the feature of single morph populations, there was a high variability in reproductive success between populations such as the number of seeds per ramet (425–2633), the number of flowers per ramet (9–36) and the mean weight of seeds (0.03–0.17 mg). Small populations and even those consisting of only one style morph may show a high reproductive success. As a whole, H. palustris showed a negative relationship of reproductive success with the surface area of its populations.     

A courtship advantage for small males in Drosophila subobscura

Large male Drosophila subobscura carry bigger drops of regurgitated food during courtship and have greater courtship success with starved females than do small males. However, if males are prevented from producing a drop, the small males have greater courtship success than the large males, suggesting that they perform some other aspect of courtship better than large males. In the present study small males were better than large ones at tracking the female during the courtship dance. Although males of different sizes ran at the same top speed during the dance, the larger males lagged further behind the female presumably because they take longer to accelerate to or decelerate from any given speed. A male's walking ability will also depend on other factors such as his ‘athletic ability’ and the amount of food stored in his crop and body tissues. The possible relationships between athletic and food gathering ability and fertility in wild males are discussed.     

Pollen quantity and quality as explanations for low seed set in small populations exemplified by Eupatorium (Asteraceae)

As plant populations decrease in size, reduced seed set may contribute to their ultimate extirpation. In this study, effects of pollen quantity and compatibility relationships (quality) on seed set were investigated in a rare species (Eupatorium resinosum) and a closely related common species (E. perfoliatum). The impact of pollen quantity was studied through pollen supplementation experiments in two populations of each species. Addition of pollen increased seed set only in the smaller population of E. resinosum. Compatibility relationships (pollen quality) were investigated in a diallel crossing experiment using ten genotypes from the same populations. Plants from the smaller population of E. resinosum were found to be 40% cross-incompatible, which was higher than the larger population of E. resinosum and the two populations of E. perfoliatum, the latter showing signs of self-compatibility in some individuals. In addition the variance in number of compatible matings per individual was higher in the smaller population of E. resinosum. These results are consistent with a computer simulation model that investigated the effect of small population size on S-allele diversity. Sufficient pollination accompanied by a partial breakdown of the incompatibility system may account, in part, for the relative success of E. perfoliatum.     

Familial versus mass selection in small populations

We used diffusion approximations and a Markov-chain approach to investigate the consequences of familial selection on the viability of small populations both in the short and in the long term. The outcome of familial selection was compared to the case of a random mating population under mass selection. In small populations, the higher effective size, associated with familial selection, resulted in higher fitness for slightly deleterious and/or highly recessive alleles. Conversely, because familial selection leads to a lower rate of directional selection, a lower fitness was observed for more detrimental genes that are not highly recessive, and with high population sizes. However, in the long term, genetic load was almost identical for both mass and familial selection for populations of up to 200 individuals. In terms of mean time to extinction, familial selection did not have any negative effect at least for small populations (N ≤ 50). Overall, familial selection could be proposed for use in management programs of small populations since it increases genetic variability and short-term viability without impairing the overall persistence times.     

Pseudopregnancy and aseasonal breeding in dairy goats: genetic basis of fertility and impact on lifetime productivity

Until recently, the main selection focus in UK dairy goats has been on milk yield. To develop a selection index suitably weighted for a variety of traits, it is important to understand the genetic relationships between production, health and fertility traits. This study focussed on three aspects of reproduction that are of interest to goat breeders. (1) Out of season (OOS) kidding ability: goats are highly seasonal breeders so achieving consistent, year-round dairy production presents a challenge. It may be possible to select for extended or shifted breeding cycles, however, there are no published studies on the genetic basis of seasonal kidding ability, and a genetic correlation with milk production in dairy goats; (2) age at first kidding (AFK): a reduced AFK offers the opportunity for more rapid genetic improvement, as well as reducing the amount of time and resources required to raise the animals to producing age; (3) pseudopregnancy (PPG): as it is difficult to diagnose pregnancy within 30 days of mating, high herd levels of PPG could add a significant delay in breeding replacement animals, or commencing a new lactation. Using records from 9546 goats, the objective of this study was to investigate the genetic relationships between the reproductive traits described above, and the production traits 520-day milk yield (MY520), lifetime milk yield (MYLife) and lifetime number of days in milk (DIMLife). The ‘out of season’ phenotype was defined as week of kidding relative to the 4 weeks of the year where the highest average number of births occur. Incidences of PPG that occurred during the first lactation were used as cases, while goats with none were assigned as controls. Relevant fixed and random effects were fitted in the models. In line with other reproduction traits, heritability estimates were low ranging from 0.08 to 0.11. A negative genetic correlation was found between AFK and MY520 (−0.22±0.10), whereas a positive genetic correlation was found between PPG and DIMLife (0.58±0.11). Pseudopregnancy and OOS were positively genetically correlated (0.36±0.15). All other genetic correlations were very low. The results of this study indicate that selection for the reproductive traits analysed is feasible, without adversely affecting MYLife.     

Selection,linkage, and dominance in small populations

Summary Linkage, dominance, and selection interact significantly to alter the mean coefficient of inbreeding. The effect of one is not predictable without the other two. Close linkage between adjacent loci in the presence of intense selection caused a different response with overdominant gene action from with partial dominance. When selection was random, effects of linkage and dominance on the coefficient of inbreeding were nonexistent; but when selection was by either phenotype or genotype, linkage and dominance became important. Joint effects between linkage, dominance, and selection are illustrated in specific simulated populations.     

Uncertainty analysis of the productivity of cattle populations in tropical drylands

This article presents an uncertainty analysis of the productivity of cattle herds in traditional farming systems of West and Central African drylands. The study focused on productivity rates in animal numbers (RN) and meat weights (RW) estimated from a herd growth model, which were compared with FAOSTAT-based estimates. The uncertainty analysis contained the following two steps: uncertainty propagation and a global sensitivity analysis. The analysis was based on a state-of-the-art of the current knowledge and a set of available data on the herd performances. The calculations used Monte Carlo simulations to estimate the 95% confidence intervals (CI) of RN and RW and the standardized regression coefficients method to estimate the contribution of the input variables to the outputs variances. The mean rate RN was estimated to 0.127 animal/animal-year with a 95% CI of (0.091, 0.163) and the mean rate RW to 11.7 kg/animal-year with a 95% CI of (8.8, 14.7), corresponding to relative variation around the mean of about ±29% and ±25%, respectively. The input variables that contributed most to the variance of RN (almost 76% of the output variance) were the calving rate, the adult female mortality rate and the female proportion in the population (determined by the pattern of the male offtake in the herds). The input variables that contributed most to the variance of RW were the same as those for RN plus the adult live weights. The CI ranges that were estimated in this article indicate that productivity rates based on literature data or expert estimations of the herd performances should be considered with caution. Research efforts based on gold-standard herd monitoring protocols accounting for temporal and spatial variations should be undertaken in future to decrease the knowledge gaps on the input variables that contribute most to these ranges.