Local extinction and recolonization, species effective population size, and modern human origins

A primary objection from a population genetics perspective to a multiregional model of modern human origins is that the model posits a large census size, whereas genetic data suggest a small effective population size. The relationship between census size and effective size is complex, but arguments based on an island model of migration show that if the effective population size reflects the number of breeding individuals and the effects of population subdivision, then an effective population size of 10,000 is inconsistent with the census size of 500,000 to 1,000,000 that has been suggested by archeological evidence. However, these models have ignored the effects of population extinction and recolonization, which increase the expected variance among demes and reduce the inbreeding effective population size. Using models developed for population extinction and recolonization, we show that a large census size consistent with the multiregional model can be reconciled with an effective population size of 10,000, but genetic variation among demes must be high, reflecting low interdeme migration rates and a colonization process that involves a small number of colonists or kin-structured colonization. Ethnographic and archeological evidence is insufficient to determine whether such demographic conditions existed among Pleistocene human populations, and further work needs to be done. More realistic models that incorporate isolation by distance and heterogeneity in extinction rates and effective deme sizes also need to be developed. However, if true, a process of population extinction and recolonization has interesting implications for human demographic history.     

Estimating population size by genotyping faeces.

Population size is a fundamental biological parameter that is difficult to estimate. By genotyping coyote (Canis latrans) faeces systematically collected in the Santa Monica Mountains near Los Angeles, California, we exemplify a general, non-invasive method to census large mammals. Four steps are involved in the estimation. First, presumed coyote faeces are collected along paths or roadways where coyotes, like most carnivores, often defaecate and mark territorial boundaries. Second, DNA is extracted from the faeces and species identity and sex is determined by mitochondrial DNA and Y-chromosome typing. Third, hypervariable microsatellite loci are typed from the faeces. Lastly, rarefaction analysis is used to estimate population size from faecal genotypes. This method readily provides a point count estimate of population size and sex ratio. Additionally, we show that home range use paternity and kinship can be inferred from the distribution and relatedness patterns of faecal genotypes.     

Population dynamics of large and small mammals

We offer an evaluation of the Caughley and Krebs hypothesis that small mammals are more likely than large mammals to possess intrinsic population regulating mechanisms. Based on the assumption that intrinsic regulation will be manifest via direct density-dependent feedbacks, and extrinsic regulation via delayed density-dependent feedbacks, we fit autoregressive models to 30 time series of abundance for large and small mammals to characterize their dynamics. Delayed feedbacks characterizing extrinsic mechanisms, such as trophic-level interactions, were detected in most time series, including both small and large mammals. Spectral analyses indicated that the effect of such delayed feedbacks on the variability in population growth rates differed with body size, with large mammals exhibiting predominantly reddened and whitened spectra in contrast with predominantly blue spectra for small mammals. Large mammals showed less variance and more stable dynamics than small mammals, consistent with, among other factors, differences in their potential population growth rates. Patterns of population dynamics in small versus large mammals contradicted those predicted by the Caughley and Krebs hypothesis.     

The consequences of the variance-mean rescaling effect on effective population size

The effective population size (N_e), and the ratio between N_e and census population size (N) are often used as measures of population viability. We show that using the harmonic mean of population sizes over time – a common proxy for N_e– has some important evolutionary consequences and implications for conservation management. This stems from the fact that there is no unambiguous relationship between the arithmetic and harmonic means for populations fluctuating in size. As long as the variance of population size increases moderately with increasing arithmetic mean population size, the harmonic mean also increases. However, if the variance of population size increases more rapidly, which existing data often suggest, then the harmonic mean may actually decrease with increasing arithmetic mean. Thus maximizing N may not maximize N_e, but could instead lower the adaptive potential and hence limit the evolutionary response to environmental change. Large census size has the clear advantage of lowering demographic stochasticity, and hence extinction risk, and under certain conditions large census size also minimizes the loss of genetic variation. Consequently, maximising census size has served as a useful dogma in ecology, genetics and conservation. Nonetheless, due to the intricate relationships among N_e, population viability and the properties of population fluctuations, we suggest that this dogma should be taken only as a rule of thumb.     

The genetic effective and adult census size of an Australian population of tiger prawns (Penaeus esculentus)

This study compares estimates of the census size of the spawning population with genetic estimates of effective current and long-term population size for an abundant and commercially important marine invertebrate, the brown tiger prawn (Penaeus esculentus). Our aim was to focus on the relationship between genetic effective and census size that may provide a source of information for viability analyses of naturally occurring populations. Samples were taken in 2001, 2002 and 2003 from a population on the east coast of Australia and temporal allelic variation was measured at eight polymorphic microsatellite loci. Moments-based and maximum-likelihood estimates of current genetic effective population size ranged from 797 to 1304. The mean long-term genetic effective population size was 9968. Although small for a large population, the effective population size estimates were above the threshold where genetic diversity is lost at neutral alleles through drift or inbreeding. Simulation studies correctly predicted that under these experimental conditions the genetic estimates would have non-infinite upper confidence limits and revealed they might be overestimates of the true size. We also show that estimates of mortality and variance in family size may be derived from data on average fecundity, current genetic effective and census spawning population size, assuming effective population size is equivalent to the number of breeders. This work confirms that it is feasible to obtain accurate estimates of current genetic effective population size for abundant Type III species using existing genetic marker technology.     

Measuring species diversity while counting large mammals: comparison of methods using species-accumulation curves

With a growing need for wildlife conservation and management in the communal lands of Africa, comprehensive ecological monitoring tools need to be developed and evaluated. While wildlife census methods are often compared in terms of precision and accuracy to estimate the population size of various target species, little attention has been paid to the measure of species diversity in mammal communities. A combined measure of abundance and community composition is, however, a crucial source of information in determining conservation priorities and to evaluate the ecosystem responses to management activities. In this study, we present five census methods of large to medium‐sized mammals and compare their efficacy in measuring species diversity. A species accumulation curve analysis is used with a predictive model to estimate the local species richness, the level of completeness of our censuses as well as the effort required to carry out a census. Advantages and limits of each method are discussed through comparison of their respective measure of species richness and their species accumulation rate. Results illustrate a large difference between methods in the ability for species detection, with censuses completed by bicycle offering the best option within the context of a unprotected area.     

Environmental Fluctuations and Level of Density-Compensation Strongly Affects the Probability of Fixation and Fixation Times

The probability of, and time to, fixation of a mutation in a population has traditionally been studied by the classic Wright–Fisher model where population size is constant. Recent theoretical expansions have covered fluctuating populations in various ways but have not incorporated models of how the environment fluctuates in combination with different levels of density-compensation affecting fecundity. We tested the hypothesis that the probability of, and time to, fixation of neutral, advantageous and deleterious mutations is dependent on how the environment fluctuates over time, and on the level of density-compensation. We found that fixation probabilities and times were dependent on the pattern of autocorrelation of carrying capacity over time and interacted with density-compensation. The pattern found was most pronounced at small population sizes. The patterns differed greatly depending on whether the mutation was neutral, advantageous, or disadvantageous. The results indicate that the degree of mismatch between carrying capacity and population size is a key factor, rather than population size per se, and that effective population sizes can be very low also when the census population size is far above the carrying capacity. This study highlights the need for explicit population dynamic models and models for environmental fluctuations for the understanding of the dynamics of genes in populations.     

Using sample aerial surveys to estimate the abundance of the endangered Grevy’s zebra in northern Kenya

The effective management of endangered mammals requires reliable estimates of population size. This is challenging for species such as Grevy’s zebra (Equus grevyi) that are distributed over large areas at low densities. Less than 2500 Grevy’s zebra remain in the wild, scattered across 85,000 km² of savannah in northern Kenya and Ethiopia. An efficient, accurate and repeatable survey method is required to guide conservation planning for the species. Currently, total aerial counts are used to census endangered species within Kenya, but are costly in terms of resources. In this study, we evaluated the suitability of sample survey methods for Grevy’s zebra. We estimated population size using sample aerial counts for a known population of Grevy’s zebra in Lewa Wildlife Conservancy (LWC), providing the opportunity to test the accuracy of sample methods, while comparing resource costs with total count methods. We sampled one‐third of LWC using parallel 500‐ m strip transects at 1500‐ m intervals. The population estimate was comparable to the known population size and was less than half as expensive as the equivalent total count survey. Our results suggest sample aerial surveys provide an accurate and cost‐effective means of monitoring Grevy’s zebra and other endangered species in open habitats.     

Inferred Paternity and Male Reproductive Success in a Killer Whale (Orcinus orca) Population

We used data from 78 individuals at 26 microsatellite loci to infer parental and sibling relationships within a community of fish-eating ("resident") eastern North Pacific killer whales (Orcinus orca). Paternity analysis involving 15 mother/calf pairs and 8 potential fathers and whole-pedigree analysis of the entire sample produced consistent results. The variance in male reproductive success was greater than expected by chance and similar to that of other aquatic mammals. Although the number of confirmed paternities was small, reproductive success appeared to increase with male age and size. We found no evidence that males from outside this small population sired any of the sampled individuals. In contrast to previous results in a different population, many offspring were the result of matings within the same "pod" (long-term social group). Despite this pattern of breeding within social groups, we found no evidence of offspring produced by matings between close relatives, and the average internal relatedness of individuals was significantly less than expected if mating were random. The population's estimated effective size was <30 or about 1/3 of the current census size. Patterns of allele frequency variation were consistent with a population bottleneck.     

Social Spacing in Small Mammals: Patterns of Individual Variation

The pattern of social spacing in small mammals differs fromthat observed in many other vertebrates. Small mammals frequentlyhave non-exclusive territories and tolerate a large amount ofoverlap with other conspecifics. The determinant factors ofhome range or territory size in small mammals are not knownfor most species. We carried out a study of the determinantfactors of home range size in a model small mammal, the easternchipmunk, Tamias striatus. The population was studied for fiveyears. The effect of experimental perturbations on food supplyand population density offered strong evidence that the meanhome range size in the population was determined by resourceabundance. Changes in population density had little or no measurableeffect. We noted that even when mean home range size decreasedsignificantly in response to an increase in available food,a great deal of variability in individual home range sizes remained.We hypothesized that this pattern of variation among individualswas also resource related; large home ranges would be locatedin areas of low resource density and small home ranges wouldbe located in areas of high resource density. Our data to datedo not offer support for this hypothesis; however our researchhas shown that the data needed to convincingly reject the nullhypothesis are very complex. We discuss the evidence requiredto study patterns of individual variation, and how models ofoptimal territory size may be useful. Research that examinespatterns of individual variation are few in number, yet studiesof individual variation will ultimately provide the best insightson the dynamics of evolutionary ecology.     

Male reproductive competition in spawning aggregations of cod (Gadus morhua, L.)

Reproductive competition may lead to a large skew in reproductive success among individuals. Very few studies have analysed the paternity contribution of individual males in spawning aggregations of fish species with huge census population sizes. We quantified the variance in male reproductive success in spawning aggregations of cod under experimental conditions over an entire spawning season. Male reproductive success was estimated by microsatellite-based parentage analysis of offspring produced in six separate groups of spawning cod. In total, 1340 offspring and 102 spawnings distributed across a spawning season were analysed. Our results show that multiple males contributed sperm to most spawnings but that paternity frequencies were highly skewed among males, with larger males on average siring higher proportions of offspring. It was further indicated that male reproductive success was dependent on the magnitude of the size difference between a female and a male. We discuss our results in relation to the cod mating system. Finally, we suggest that the highly skewed distribution of paternity success observed in cod may be a factor contributing to the low effective population size/census population size ratios observed in many marine organisms.     

Factors affecting levels of genetic diversity in natural populations.

Genetic variability is the clay of evolution, providing the base material on which adaptation and speciation depend. It is often assumed that most interspecific differences in variability are due primarily to population size effects, with bottlenecked populations carrying less variability than those of stable size. However, we show that population bottlenecks are unlikely to be the only factor, even in classic case studies such as the northern elephant seal and the cheetah, where genetic polymorphism is virtually absent. Instead, we suggest that the low levels of variability observed in endangered populations are more likely to result from a combination of publication biases, which tend to inflate the level of variability which is considered ''normal'', and inbreeding effects, which may hasten loss of variability due to drift. To account for species with large population sizes but low variability we advance three hypotheses. First, it is known that certain metapopulation structures can result in effective population sizes far below the census size. Second, there is increasing evidence that heterozygous sites mutate more frequently than equivalent homozygous sites, plausibly because mismatch repair between homologous chromosomes during meiosis provides extra opportunities to mutate. Such a mechanism would undermine the simple relationship between heterozygosity and effective population size. Third, the fact that related species that differ greatly in variability implies that large amounts of variability can be gained or lost rapidly. We argue that such cases are best explained by rapid loss through a genome-wide selective sweep, and suggest a mechanism by which this could come about, based on forced changes to a control gene inducing coevolution in the genes it controls. Our model, based on meiotic drive in mammals, but easily extended to other systems, would tend to facilitate population isolation by generating molecular incompatabilities. Circumstances can even be envisioned in which the process could provide intrinsic impetus to speciation.     

The Quasispecies for the Wright–Fisher Model

We consider the classical Wright–Fisher model of population genetics. We prove the existence of an error threshold for the mutation probability per nucleotide, below which a quasispecies is formed. We show a new phenomenon, specific to a finite population model, namely the existence of a population threshold: to ensure the stability of the quasispecies, the population size has to be at least of the same order as the genome length. We derive an explicit formula describing the quasispecies.     

Temporal genetic variation of mitochondrial DNA and the female effective population size of red drum (Sciaenops ocellatus) in the northern Gulf of Mexico

We studied genetic drift of mitochondrial DNA (mtDNA) haplotype frequencies in a natural population of red drum (Sciaenops ocellatus) from the northern Gulf of Mexico (Gulf). The amount of genetic drift observed across temporally adjacent year classes (1986–89) was used to estimate variance effective (female) population size (N_ef). N_ef was estimated to be 14 308 and the ratio of female effective size to adult female census size was approximately 0.004, which is among the lowest value reported for vertebrate animals. Low effective size relative to census size among red drum in the northern Gulf may result from yearly fluctuations in the number of breeding females, high variance in female reproductive success, or both. Despite low genetic effective size relative to census size, the genetic effective population size of red drum in the northern Gulf appears sufficiently large to preclude potentially deleterious effects of inbreeding.     

Genome size and developmental parameters in the homeothermic vertebrates.

Although unrelated to any intuitive notions of organismal complexity, haploid genome sizes (C values) are correlated with a variety of cellular and organismal parameters in different taxa. In some cases, these relationships are universal--notably, genome size correlates positively with cell size in each of the vertebrate classes. Other relationships are apparently relevant only in particular groups. For example, although genome size is inversely correlated with metabolic rate in both mammals and birds, no such relationship is found in amphibians. More recently, it has been suggested that developmental rate and (or) longevity are related to genome size in birds. In the present study, a large dataset was used to examine possible relationships between genome size and various developmental parameters in both birds and mammals. In neither group does development appear to be of relevance to genome size evolution (except perhaps indirectly in birds through the intermediation of body size and (or) within the rodents), a situation very different from that found in amphibians. These findings make it clear that genome size evolution cannot be understood without reference to the particular biology of the organisms under study.     

Cell size does not always correspond to genome size: phylogenetic analysis in geckos questions optimal DNA theories of genome size evolution

At higher taxonomic levels, a significant correlation between genome size (GS) and erythrocyte size (ES) has been reported for many taxa. Under optimal DNA theories, several mechanisms presuming a causative link between GS and ES have been proposed to explain this seemingly general pattern. The correlation between GS and ES has been rarely tested among closely related organisms within an explicit phylogenetic framework. Eyelid geckos (family Eublepharidae) serve as a proper group to conduct such an analysis. We used flow cytometry to measure GS in 15 forms of eublepharids and conducted a phylogenetic reconstruction of GS and ES to test the successiveness of evolutionary shifts in these traits. Most parsimoniously, there were two independent increases and two decreases in GS during the evolution of eublepharids. Nevertheless, changes in GS and ES were not phylogenetically associated in a manner predicted by optimal DNA theories. Our results question the generality of causative bonds between DNA content and cell size and demonstrate that cell size cannot always serve as a proxy of GS. We suggest there is no need to expect a direct causative link between GS and ES to explain the correlation between GS and cell size at higher taxonomic levels. Such a correlation can be explained by simple mechanistic constraints and a combination of the population-genetic model of genome complexity with cell-size-metabolic rate relationship.     

Red squirrels decline in abundance in the boreal forests of Finland and NW Russia

Recent global warming and other anthropogenic changes have caused well‐documented range shifts and population declines in many species over a large spatial extent. Most large‐scale studies focus on birds, large mammals, and threatened species, whereas large‐scale population trends of small to medium‐sized mammals and species that are currently of least concern remain poorly studied. Large‐scale studies are needed because on a smaller scale, important patterns may be masked by local variation and stochastic processes. Here, we utilized snow track census data from Finland and NW Russia to estimate population growth rates of the Eurasian red squirrel Sciurus vulgaris for a period of 17 yr in an area of over 1 000 000 km². We also studied the effects of changes in summer and winter temperatures, winter precipitation, predator abundance, and canopy cover on estimated red squirrel population growth rates. Our results suggest that red squirrel populations have declined in most parts of the study area, the only remarkable exception being SW Russia. These results are in concordance with previous studies suggesting that species that are still common and of least concern may be declining. However, our findings are in contrast to the common pattern of northern populations of boreal species increasing due to global warming. The estimated population growth rates are in synchrony over vast areas, suggesting that the underlying reasons also operate on a large scale. We indeed find that the population growth rate was lower in regions where winters warmed faster during the study period, suggesting that changes in the environment (or biotic changes associated with it) are linked with the decline of red squirrels.     

Genome size and metabolic intensity in tetrapods: a tale of two lines

We show the negative link between genome size and metabolic intensity in tetrapods, using the heart index (relative heart mass) as a unified indicator of metabolic intensity in poikilothermal and homeothermal animals. We found two separate regression lines of heart index on genome size for reptiles-birds and amphibians-mammals (the slope of regression is steeper in reptiles-birds). We also show a negative correlation between GC content and nucleosome formation potential in vertebrate DNA, and, consistent with this relationship, a positive correlation between genome GC content and nuclear size (independent of genome size). It is known that there are two separate regression lines of genome GC content on genome size for reptiles-birds and amphibians-mammals: reptiles-birds have the relatively higher GC content (for their genome sizes) compared to amphibians-mammals. Our results suggest uniting all these data into one concept. The slope of negative regression between GC content and nucleosome formation potential is steeper in exons than in non-coding DNA (where nucleosome formation potential is generally higher), which indicates a special role of non-coding DNA for orderly chromatin organization. The chromatin condensation and nuclear size are supposed to be key parameters that accommodate the effects of both genome size and GC content and connect them with metabolic intensity. Our data suggest that the reptilian-birds clade evolved special relationships among these parameters, whereas mammals preserved the amphibian-like relationships. Surprisingly, mammals, although acquiring a more complex general organization, seem to retain certain genome-related properties that are similar to amphibians. At the same time, the slope of regression between nucleosome formation potential and GC content is steeper in poikilothermal than in homeothermal genomes, which suggests that mammals and birds acquired certain common features of genomic organization.     

Paternity assignment and demographic closure in the New Zealand southern right whale

The identification and characterization of reproductively isolated subpopulations or 'stocks' are essential for effective conservation and management decisions. This can be difficult in vagile marine species like marine mammals. We used paternity assignment and 'gametic recapture' to examine the reproductive autonomy of southern right whales (Eubalaena australis) on their New Zealand (NZ) calving grounds. We derived DNA profiles for 34 mother-calf pairs from skin biopsy samples, using sex-specific markers, 13 microsatellite loci and mtDNA haplotypes. We constructed DNA profiles for 314 adult males, representing 30% of the census male abundance of the NZ stock, previously estimated from genotypic mark-recapture modelling to be 1085 (95% CL 855, 1416). Under the hypothesis of demographic closure and the assumption of equal reproductive success among males, we predict: (i) the proportion of paternities assigned will reflect the proportion of the male population sampled and (ii) the gametic mark-recapture (GMR) estimate of male abundance will be equivalent to the census male estimate for the NZ stock. Consistent with these predictions, we found that the proportion of assigned paternities equalled the proportion of the census male population size sampled. Using the sample of males as the initial capture, and paternity assignment as the recapture, the GMR estimate of male abundance was 1001 (95% CL 542, 1469), similar to the male census estimate. These findings suggest that right whales returning to the NZ calving ground are reproductively autonomous on a generational timescale, as well as isolated by maternal fidelity on an evolutionary timescale, from others in the Indo-Pacific region.     

Strength of density feedback in census data increases from slow to fast life histories

Life-history theory predicts an increasing rate of population growth among species arranged along a continuum from slow to fast life histories. We examine the effects of this continuum on density-feedback strength estimated using long-term census data from >700 vertebrates, invertebrates, and plants. Four life-history traits (Age at first reproduction, Body size, Fertility, Longevity) were related statistically to Gompertz strength of density feedback using generalized linear mixed-effects models and multi-model inference. Life-history traits alone explained 10 to 30% of the variation in strength across species (after controlling for time-series length and phylogenetic nonindependence). Effect sizes were largest for body size in mammals and longevity in birds, and density feedback was consistently stronger for smaller-bodied and shorter-lived species. Overcompensatory density feedback (strength <-1) occurred in 20% of species, predominantly at the fast end of the life-history continuum, implying relatively high population variability. These results support the idea that life history leaves an evolutionary signal in long-term population trends as inferred from census data. Where there is a lack of detailed demographic data, broad life-history information can inform management and conservation decisions about rebound capacity from low numbers, and propensity to fluctuate, of arrays of species in areas planned for development, harvesting, protection, and population recovery.