Mechanisms of density dependence in fluctuating vole populations: deducing annual density dependence from seasonal processes

Based on recent advances in time-series analyses of ecological dynamics using statistical and mathematical models, we summarise our recent results on the seasonal processes in the annual population dynamics of the grey-sided vole Clethrionomys rufocanus (Sundevall, 1846) in Hokkaido, Japan, and report additional analyses on annual and seasonal density dependence. Annual direct density dependence was strong in almost all populations. In contrast, delayed density dependence was generally weak, although clear delayed density dependence was detected in some of the studied populations. Although seasonal density dependence was observed both in winter and summer, direct density dependence was much more profound during winter; thus, winter density dependence contributed most to the overall annual direct density dependence. We found no correlation between the seasonal components of annual direct density dependence; however, the corresponding seasonal components for annual delayed density dependence were positively correlated. We conclude that winter conditions influence the strength of annual direct density dependence most profoundly. Moreover, we conclude that direct density dependence during summer and winter may be generated by different mechanisms, whereas delayed density dependence seems to be generated by a common mechanism. Candidate mechanisms are discussed in relation to general knowledge of northern rodent populations and to specific insights provided by earlier studies of grey-sided voles in Hokkaido.     

The importance of control populations for the identification and management of genetic diversity

A fundamental criterion for recognizing species or populations as potentially endangered is the presence/absence of genetic diversity. However, the lack of control populations in many studies of natural systems deprives one from unambiguous criteria for evaluating the genetic effects of small population size and its potential effects on fitness. In this study, I present an example of how the lack of adequate controls may lead to erroneous conclusions for understanding the role that population size may play in the preservation of genetic diversity and fitness of natural populations. The genetic analysis of a population of greater prairie chickens from Illinois, USA, between two time periods (1974–1987 and 1988–1993) in which the studied population experienced a substantial reduction in size and fitness showed no apparent associations between population size and genetic diversity. However, genetic analysis of museum specimens from early this century indicated that Illinois prairie chickens had originally higher levels of genetic diversity, which suggest the Illinois population was already bottlenecked by the 1970s. This study emphasizes the importance of using historical controls to evaluate the temporal dynamics of genetic variability in natural populations. The large number of museum collections worldwide may provide a valuable source of genetic information from past populations, particularly in species currently endangered as a result of human activities. This revised version was published online in July 2006 with corrections to the Cover Date.     

Role of individual dispersal in genetic resilience in fluctuating populations of the gray‐sided vole Myodes rufocanus

Population densities of the gray‐sided vole Myodes rufocanus fluctuate greatly within and across years in Japan. Here, to investigate the role of individual dispersal in maintaining population genetic diversity, we examined how genetic diversity varied during fluctuations in density by analyzing eight microsatellite loci in voles sampled three times per year for 5 years, using two fixed trapping grids (approximately 0.5 ha each). At each trapping session, all captured voles at each trapping grid were removed. The STRUCTURE program was used to analyze serially collected samples to examine how population crashes were related to temporal variability, based on local‐scale genetic compositions in each population. In total, 461 and 527 voles were captured at each trapping grid during this study. The number of voles captured during each trapping session (i.e., vole density) varied considerably at both grids. Although patterns in fluctuations were not synchronized between grids, the peak densities were similar. At both grids, the mean allele number recorded at each trapping session was strongly, positively, and nonlinearly correlated with density. STRUCTURE analyses revealed that the proportions of cluster compositions among individuals at each grid differed markedly before and after the crash phase, implying the long‐distance dispersal of voles from remote areas at periods of low density. The present results suggest that, in gray‐sided vole populations, genetic diversity varies with density largely at the local scale; in contrast, genetic variation in a metapopulation is well‐preserved at the regional scale due to the density‐dependent dispersal behaviors of individuals. By influencing the dispersal patterns of individuals, fluctuations in density affect metapopulation structure spatially and temporally, while the levels of genetic diversity are preserved in a metapopulation.     

The effective size of annual plant populations: the interaction of a seed bank with fluctuating population size in maintaining genetic variation

Many annual plant populations undergo dramatic fluctuations in size. Such fluctuations can result in the loss of genetic variability. Here I formalize the potential for a seed bank to buffer against such genetic loss. The average time to seed germination (T) defines the generation time of "annuals" with a seed bank, and assuming random seed germination, I show that, under otherwise ideal conditions, a population's effective size (Ne) equals NT, where N is the number of adult plants. This result supports the general principle that lengthening the prereproductive period increases Ne. When adult numbers vary, Ne at any time depends on N and on the numbers contributing to the seed bank in previous seasons. Averaging these effects over time gives Ne approximately Nh + (T - 1)Na, where Nh and Na are the harmonic and arithmetic means of the adult population. Thus if T > 1, Ne is determined primarily by Na. Simulations showed that until fluctuations in N are large (>25x) this relationship is accurate. I extended the theory to incorporate a selfing rate (S) and reproductive variance (I) through seed production (k), outcrossed pollen (m), and variation in selfing rate: Ne = NT(1 -S/2)/(1 + I) = NT/[1 + FIS)(1 + I)]. Reproductive variance (I) equals [Ik(1 + S)2 + IM(1 - S)2 + 2(1 - S2)Ikm = S2IS(1 + Ik)]/4, , where Ij is the standardized variance (Vj/j2) of factor j and Ikm is the standardized covariance between k and m. These results are applicable to other organisms with a similar life history, such as freshwater crustaceans with diapausing eggs (e.g., tadpole shrimp, clam shrimp, and fairy shrimp) and other semelparous species with discrete breeding seasons and a variable maturation time (e.g., Pacific salmon).     

Somatic generation of a genetic polymorphism: towards the solution of the I-J enigma

I-J has been regarded as a polymorphic genetic marker controlled by a locus in the major histocompatibility complex (MHC) which is expressed only on functional T cells. However, this antigenic determinant has been found not to be directly encoded by the MHC gene per se but is somatically generated according to the MHC of the cellular environment during ontogeny. This explains the apparent linkage of I-J to MHC, despite the failure to find the structural gene for I-J within the MHC. The I-J paradox provides an instance of a polymorphism that does not follow the standard genetics of Mendelian structural genes.     

Heritable genetic variation via mutation-selection balance: Lerch's zeta meets the abdominal bristle

Most quantitative traits in most populations exhibit heritable genetic variation. Lande proposed that high levels of heritable variation may be maintained by mutation in the face of stabilizing selection. Several analyses have appeared of two distinct models with n additive polygenic loci subject to mutation and stabilizing selection. Each is reviewed and a new analysis and model are presented. Lande and Fleming analyzed extensions of a model originally treated by Kimura which assumes a continuum of possible allelic effects at each locus. Latter and Bulmer analyzed a model with diallelic loci. The published analyses of these models lead to qualitatively different predictions concerning the dependence of the equilibrium genetic variance on the underlying biological parameters. A new asymptotic analysis of the Kimura model shows that the different predictions are not consequences of the number of alleles assumed but rather are attributable to assumptions concerning the relative magnitudes of per locus mutation rates, the phenotypic effects of mutation, and the intensity of selection. This conclusion is reinforced by analysis of a model with triallelic loci. None of the approximate analyses presented are mathematically rigorous. To quantify their accuracy and display the domains of validity for alternative approximations, numerically determined equilibria are presented. In addition, empirical estimates of mutation rates and selection intensity are reviewed, revealing weaknesses in both the data and its connection to the models. Although the mathematical results and underlying biological requirements of my analyses are quite different from those of Lande, the results do not refute his hypothesis that considerable additive genetic variance may be maintained by mutation-selection balance. However, I argue that the validity of this hypothesis can only be determined with additional data and mathematics.     

High genetic diversity and strong differentiation in dramatically fluctuating populations of Zostera japonica (Zosteraceae): implication for conservation

Aims Seagrasses provide a variety of ecosystem goods and services, but they are subjected to frequently anthropogenic disturbances. In this study, we genotyped samples collected fromZostera japonicameadows with dramatic fluctuations in the area in order to understand the distribution of genetic variation within and among populations.     

The blowfly's dance: Role in the regulation of food intake

Blowflies that have been deprived of sugar are known to execute a ‘dance’ that consists of walking in a roughly spiral path while repeatedly extending the proboscis, when their taste receptors encounter sugar.This dance can also be elicited by water or crude protein extracts, which along with sugars constitute the major feeding stimulants for the blowfly. The intensity of the dance, as measured by the distance walked in a spiral path, is a function of the fly's state of deprivation with respect to the eliciting stimulus, and of the concentration of the stimulating solution. A given feeding stimulant is capable of eliciting dancing only when the fly has been deprived of that substance. Dancing can function in the laboratory as an effective search pattern with several different patterns of food distribution. These characteristics of the dance are discussed in relation to the fly's feeding habits and the known physiological controls over its food intake, and a rôle for the dance in the regulation of food intake is suggested.     

On the neutrality of molecular genetic markers: pedigree analysis of genetic variation in fragmented populations

Many studies employ molecular markers to infer ecological and evolutionary processes, assuming that variation found at genetic loci offers a reliable representation of stochastic events in natural populations. Increasingly, evidence emerges that molecular markers might not always be selectively neutral. However, only a few studies have analysed how deviations from neutrality could affect estimates of genetic variation, using populations with known genealogy. We monitored changes in allozyme variation over eight generations in captive metapopulations of the butterfly Bicyclus anynana. Population demography was recorded by individually marking 35 000 butterflies and constructing pedigrees. We designed a computer program that simulated the inheritance of founder allozyme alleles in butterfly pedigrees. We thus tested whether the observed transmission of allozyme alleles could be explained by random genetic drift alone, or whether there was evidence for positive or negative selection. This analysis showed that in the smallest metapopulations the loss of allozyme variation exceeded the neutral rate. Possibly, linkage disequilibria between deleterious mutations and marker alleles resulted in background selection and a faster erosion of allozyme variation. In larger metapopulations, one locus (MDH) showed a significant heterozygote excess and smaller than expected loss in heterozygosity, observations consistent with (associative) overdominance. This study demonstrates that the neutrality of molecular markers cannot always be assumed, particularly in small populations with a high mutation load.     

Effect of genetic variants of OPTN in the pathophysiology of Paget's disease of bone

Paget's disease of bone (PDB) is the second most frequent metabolic bone disease after osteoporosis. Genetic factors play an important role in PDB, but to date PDB causing mutations were identified only in the Sequestosome 1 gene at the PDB3 locus. OPTN has been recently associated with PDB, however little is known about the effect of genetic variants in this gene in PDB pathophysiology. By sequencing OPTN in SQSTM1 non-carriers PDB patients we found 16 SNPs in regulatory, coding and non-coding regions. One of those was found to be associated with PDB in our cohort - rs2234968. Our results show that rs2238968 effect may be explained by a change in OPTN splicing that give rise to a predicted truncated protein. We also performed functional studies on the variants located in OPTN promoter – rs3829923 and the rare variant ? 9906 – to investigate putative regulators of OPTN. Our results show that OPTN expression seems to be regulated by SP1, RXR, E47, and the E2F family. In conclusion, our work suggests a potential pathophysiological role of SNPs in OPTN, giving a new perspective about the regulatory mechanisms of this gene. Ultimately we discovered a new variant associated with PDB in OPTN, reinforcing the relevance of this gene for the development of this bone disease.     

Hantavirus infections in fluctuating host populations: the role of maternal antibodies

Infected females may transfer maternal antibodies (MatAbs) to their offspring, which may then be transiently protected against infections the mother has encountered. However, the role of maternal protection in infectious disease dynamics in wildlife has largely been neglected. Here, we investigate the effects of Puumala hantavirus (PUUV)-specific MatAbs on PUUV dynamics, using 7 years'' data from a cyclic bank vole population in Finland. For the first time to our knowledge, we partition seropositivity data from a natural population into separate dynamic patterns for MatAbs and infection. The likelihood of young of the year carrying PUUV-specific MatAbs during the breeding season correlated positively with infection prevalence in the overwintered parent population in the preceding spring. The probability of PUUV infection varied between seasons (highest in spring, lowest in late summer) and depended on population structure, but was also, in late autumn, notably, negatively related to summer MatAb prevalence, as well as to infection prevalence earlier in the breeding season. Hence, our results suggest that high infection prevalence in the early breeding season leads to a high proportion of transiently immune young individuals, which causes delays in transmission. This suggests, in turn, that MatAb protection has the potential to affect infection dynamics in natural populations.     

On the calculation of birth rates and death rates in fluctuating populations with continuous recruitment

Summary A two-instar and a three-instar model for the calculation of birth and death rates is proposed which both use only a minimum of assumptions. It is shown that the proposed approach is a generalization of the methods of Edmondson (1960, 1968), Caswell (1972), and Paloheimo (1974). The validity of the two methods is compared with two-instar and three-instar models according to Edmondson, Caswell and Paloheimo. Since it is impossible to use field data for the comparison, a set of 27 computer simulations was run. From these simulations the true and estimated values were obtained. The comparisons showed that it is better to use the new two-instar model in an environment with no instarspecific mortality. But it is better to use three-instar models when strong instarspecific selection prevails. Among the three-instar models the best results are obtained by the method of Paloheimo when predicting birth rates of young and of adults. It proved that the bias produced by the several methods is mainly influenced by the amount of deviation from the situation of steady state.The first chapter of this paper is part of a doctoral thesis (Seitz, 1977) submitted to the University of Munich     

The rule of "one migrant per generation" and genetic differentiation in subdivided populations

The genetic differentiation in population with migration according island and two-dimensional stepping stone models was studied with simulation methods. It is shown that migration of one or few individuals per generation is insufficient for leveling differences between subpopulations in allele frequencies. Even if migration is estimated as m = 0.5 (exchange of 50 and 500 individuals per generation) statistically significant differences remain at least in the half of populations with insular structure. Spatial heterogeneity disappears completely only if m = 0.7-0.8. In case of two-dimensional step model the level of genetic differentiation is higher and statistically significant heterogeneity remains at all levels of genetic exchange including that which was estimated as m = 1.     

The importance of genetic variation for the viability of small avian populations—the Seychelles Warbler and the African Marsh Warbler

Eising, C.M., Blaakmeer, K.B. & Komdeur, J. 2000. The importance of genetic variation for the viability of small avian populations—the Seychelles Warbler and the African Marsh Warbler. Ostrich 71 (1 & 2): 304–306.

Nowadays, many natural populations have to face up to problems such as genetic drift and ‘forced’ inbreeding as a result of reduced numbers and population isolation. This is thought to have a major effect on their survival. Research on the isolated Seychelles warbler showed that fitness parameters are not negatively affected by a high inbreeding frequency and a low level of heterozygosity. However, one has to be careful to translate these results to other isolated species. It is hypothesised that the effect of ‘genetic erosion’ on fitness may be less disastrous for island species, which are used to go through narrow population bottlenecks, as compared to continental species. Conservationists should be aware of these differences between species and of the fact that the long-term prospects can be reduced by lack of adaptive genetic potential.     

Respiratory rhythm generation in rats: The importance of inhibition

Stimulation-related modifications of activity in the phrenic nerve and external and internal intercostal nerves were studied on urethane-anesthetized rats; the inspiratory medullary structures were stimulated. The activity was recorded either following microinjections of gamma-aminobutyric acid (GABA) or its derivatives into the medial parabrachial nuclei and rostral part of the ventral respiratory group of medullary neurons, or without such microinjections. Gradual dependence of activity in these nerves on the phase of the respiratory cycle was established. It was shown that the higher was the integrated inspiratory activity, the lower became the relative gain in phrenic nerve activity caused by standard stimulation. When stimulation was applied at the postinspiratory phase, the threshold stimulus intensity showed an S-like rise with an increase in integrated inspiratory activity. Microinjections of GABA or its cyclic derivatives into the parabrachial nuclear structures decreased the inhibitory effects of the latter. During the postinspiratory phase, the effect was opposite: an increase in the relative gain of inspiratory activity and drop in the threshold. The resulting data suggest that there is a two-level organization of the respiratory regulatory inhibition and that the whole respiratory neuronal network has a compartmental structure.Neirofiziologiya/Neurophysiology, Vol. 25, No. 6, pp. 420–426, November–December, 1993.     

The genetic underpinnings of population cyclicity: establishing expectations for the genetic anatomy of cycling populations

Despite extensive research into the mechanisms underlying population cyclicity, we have little understanding of the impacts of numerical fluctuations on the genetic variation of cycling populations. Thus, the potential implications of natural and anthropogenically‐driven variation in population cycle dynamics on the diversity and evolutionary potential of cyclic populations is unclear. Here, we use Canada lynx Lynx canadensis matrix population models, set up in a linear stepping‐stone, to generate demographic replicates of biologically realistic cycling populations. Overall, increasing cycle amplitude predictably reduced genetic diversity and increased genetic differentiation, with cyclic effects increased by population synchrony. Modest dispersal rates (1–3% of the population) between high and low amplitude cyclic populations did not diminish these effects suggesting that spatial variation in cyclic amplitude should be reflected in patterns of genetic diversity and differentiation at these rates. At high dispersal rates (6%) groups containing only high amplitude cyclic populations had higher diversity and lower differentiation than those mixed with low amplitude cyclic populations. Negative density‐dependent dispersal did not impact genetic diversity, but did homogenize populations by reducing differentiation and patterns of isolation by distance. Surprisingly, temporal changes in diversity and differentiation throughout a cycle were not always consistent with population size. In particular, negative density‐dependent dispersal simultaneously decreased differences in genetic diversity while increasing differences in genetic differentiation between numerical peaks and nadirs. Combined, our findings suggest demographic changes at fine temporal scales can impact genetic variation of interacting populations and provide testable predictions relating population cyclicty to genetic variation. Further, our results suggest that including realistic demographic and dispersal parameters in population genetic models and using information from temporal changes in genetic variation could help to discern complex demographic scenarios and illuminate population dynamics at fine temporal scales.