Increased rates of sequence evolution in endosymbiotic bacteria and fungi with small effective population sizes

Mutualistic, maternally transmitted endosymbiotic microorganisms undergo severe population bottlenecks at each host generation, resulting in a reduction in effective population size (Ne). Previous studies of Buchnera, the primary endosymbiont of aphids, and of several other species of endosymbiotic bacteria have shown that these species exhibit an increase in the rate of substitution of slightly deleterious mutations, among other predicted effects of increased drift due to small Ne, such as reduced codon bias. However, these studies have been limited in taxonomic scope, and it was therefore not clear whether the increase in rate is a general feature of endosymbiont lineages. Here, we test the prediction that a long-term reduction in Ne causes an increase in substitution rate using DNA sequences of the 16S rRNA gene from 13 phylogenetically independent comparisons between taxonomically diverse endosymbiotic microorganisms and their free-living relatives. Maximum likelihood and distance-based methods both indicate a significant increase in substitution rate in a wide range of bacterial and fungal endosymbionts compared to closely related free-living lineages. We use the same data set to test whether 16S genes from endosymbionts display increased A + T content, another indicator of increased genetic drift, and find that there is no significant difference in base composition between endosymbiont and nonendosymbiont 16S genes. However, analysis of an additional data set of whole bacterial genomes demonstrates that, while host-dependent bacteria have significantly increased genomic A + T content, the base content of the 16S gene tends to vary less than that of the whole genome. It is possible that selection for stability of rRNA is strong enough to overcome the effects of drift toward increased A + T content in endosymbiont 16S genes, despite the reduced effective population sizes of these organisms.     

Adaptive evolution and effective population size in wild house mice

Estimates of the proportion of amino acid substitutions that have been fixed by selection (α) vary widely among taxa, ranging from zero in humans to over 50% in Drosophila. This wide range may reflect differences in the efficacy of selection due to differences in the effective population size (N(e)). However, most comparisons have been made among distantly related organisms that differ not only in N(e) but also in many other aspects of their biology. Here, we estimate α in three closely related lineages of house mice that have a similar ecology but differ widely in N(e): Mus musculus musculus (N(e) ～ 25,000-120,000), M. m. domesticus (N(e) ～ 58,000-200,000), and M. m. castaneus (N(e) ～ 200,000-733,000). Mice were genotyped using a high-density single nucleotide polymorphism array, and the proportions of replacement and silent mutations within subspecies were compared with those fixed between each subspecies and an outgroup, Mus spretus. There was significant evidence of positive selection in M. m. castaneus, the lineage with the largest N(e), with α estimated to be approximately 40%. In contrast, estimates of α for M. m. domesticus (α = 13%) and for M. m. musculus (α = 12 %) were much smaller. Interestingly, the higher estimate of α for M. m. castaneus appears to reflect not only more adaptive fixations but also more effective purifying selection. These results support the hypothesis that differences in N(e) contribute to differences among species in the efficacy of selection.     

Advances in laying date and increasing population size suggest positive responses to climate change in Common Eiders Somateria mollissima in Iceland

Models of climate change predict that its effects on animal populations will not always be negative, but most studies indicate negative associations between changes in climate and the phenology of animal migration and reproduction. For some populations, however, climate change may render particular environments more favourable, with positive effects on population growth. We used a 30-year population dataset on over 2000 Common Eiders Somateria mollissima at a colony in southwest Iceland to examine the response of this species to climate fluctuations. Eiders are strongly dependent on suitable climatic conditions for successful reproduction and survival. Temperatures in southwest Iceland, in both winter and summer, have generally increased over the past 30 years but have shown considerable fluctuation. We show that females laid earlier following mild winters and that year-to-year variation in the number of nests was related to the temperature during the breeding season 2 years previously. Milder summers could have positive effects on breeding success and offspring survival, producing an increase in nest numbers 2 years later when most Eiders recruit into the breeding population. In this part of their range, Eiders could benefit from a general warming of the climate.     

Patterns of protein evolution in Tetrahymena thermophila: implications for estimates of effective population size

High levels of synonymous substitutions among alleles of the surface antigen SerH led to the hypothesis that Tetrahymena thermophila has a tremendously large effective population size, one that is greater than estimated for many prokaryotes (Lynch, M., and J. S. Conery. 2003. Science 302:1401-1404.). Here we show that SerH is unusual as there are substantially lower levels of synonymous variation at five additional loci (four nuclear and one mitochondrial) characterized from T. thermophila populations. Hence, the effective population size of T. thermophila, a model single-celled eukaryote, is lower and more consistent with estimates from other microbial eukaryotes. Moreover, reanalysis of SerH polymorphism data indicates that this protein evolves through a combination of vertical transmission of alleles and concerted evolution of repeat units within alleles. SerH may be under balancing selection due to a mechanism analogous to the maintenance of antigenic variation in vertebrate immune systems. Finally, the dual nature of ciliate genomes and particularly the amitotic divisions of processed macronuclear genomes may make it difficult to estimate accurately effective population size from synonymous polymorphisms. This is because selection and drift operate on processed chromosomes in macronuclei, where assortment of alleles, disruption of linkage groups, and recombination can alter the genetic landscape relative to more canonical eukaryotic genomes.     

Estimating effective population size and migration rates from genetic samples over space and time

In the past, moment and likelihood methods have been developed to estimate the effective population size (N(e)) on the basis of the observed changes of marker allele frequencies over time, and these have been applied to a large variety of species and populations. Such methods invariably make the critical assumption of a single isolated population receiving no immigrants over the study interval. For most populations in the real world, however, migration is not negligible and can substantially bias estimates of N(e) if it is not accounted for. Here we extend previous moment and maximum-likelihood methods to allow the joint estimation of N(e) and migration rate (m) using genetic samples over space and time. It is shown that, compared to genetic drift acting alone, migration results in changes in allele frequency that are greater in the short term and smaller in the long term, leading to under- and overestimation of N(e), respectively, if it is ignored. Extensive simulations are run to evaluate the newly developed moment and likelihood methods, which yield generally satisfactory estimates of both N(e) and m for populations with widely different effective sizes and migration rates and patterns, given a reasonably large sample size and number of markers.     

Behavioral responses to linear accelerations in blind goldfish

Blind goldfish were subjected to linear accelerations on a motor car and on a parallel swing. Moyements of the fish in a tank during the accelerations were recorded with a movie camera. During the horizontal acceleration, the fish aligns his longitudinal axis in a plane perpendicular to the direction of an apparent gravity with the fish's back pointing away from the direction of this apparent gravity vector. This is similar to the manner in which the fish usually aligns himself horizontally in response to the vertically downward terrestrial gravity and can therefore be termed gravity reference response. It is concluded that blind goldfish cannot distinguish between otolith displacements caused by passive tilts and equivalent otolith displacements caused by moderate inertial forces during rectilinear acceleration. With a horizontal jerk of higher magnitude, two additional responses can occur: horizontal 180° turns following tailward jerks and straight forward darting following noseward jerks.This work was supported by NASA Grant No. NGR 23-005-201.     

Response of population size to changing vital rates in random environments

Population size and population growth rate respond to changes in vital rates like survival and fertility. In deterministic environments change in population growth rate alone determines change in population size. In random environments, population size at any time t is a random variable so that change in population size obeys a probability distribution. We analytically show that, in a density-independent population, the proportional change in population size with respect to a small proportional change in a vital rate has an asymptotic normal distribution. Its mean grows linearly at a rate equal to the elasticity of the long-term stochastic growth rate λ _S while the standard deviation scales as $\sqrt t$ . Consequently, a vital rate with a larger elasticity of λ _S may produce a larger mean change in population size compared to one with a smaller elasticity of λ _S. But a given percentage change in population size may be more likely when the vital rate with smaller elasticity is perturbed. Hence, the response of population size to perturbation of a vital rate depends not only on the elasticity of the population growth rate but also on the variance in change in population size. Our results provide a formula to calculate the probability that population size changes by a given percentage that works well even for short time periods.     

The roles of ecology,behaviour and effective population size in the evolution of a community

Organismal traits such as ecological specialization and migratory behaviour may affect colonization potential, population persistence and degree of isolation, factors that determine the composition and genetic structure of communities. However, studies focusing on community assembly rarely consider these factors jointly. We sequenced 16 nuclear genes and one mitochondrial gene from Caucasian and European populations of 30 forest‐dwelling avian species that represent diverse ecological (specialist–generalist) and behavioural (migratory‐resident) backgrounds. We tested the effects of organismal traits on population divergence and community assembly in the Caucasus forest, a continental mountain island setting. We found that (i) there is no concordance in divergence times between the Caucasus forest bird populations and their European counterparts, (ii) habitat specialists tend to be more divergent than generalists and (iii) residents tend to be more divergent than migrants. Thus, specialists and residents contribute to the high level of endemism of Caucasus forest avifauna more than do generalists and migrants. Patterns of genetic differentiation are better explained by differences in effective population sizes, an often overlooked factor in comparative studies of phylogeography and speciation, than by divergence times or levels of gene flow. Our results suggest that the Caucasus forest avifauna was assembled through time via dispersal and/or multiple vicariant events, rather than originating simultaneously via a single isolation event. Our study is one of the first multilocus, multispecies analyses revealing how ecological and migratory traits impact the evolutionary history of community formation on a continental island.     

Testing demographic models of effective population size

Due to practical difficulties in obtaining direct genetic estimates of effective sizes, conservation biologists have to rely on so-called 'demographic models' which combine life-history and mating-system parameters with F-statistics in order to produce indirect estimates of effective sizes. However, for the same practical reasons that prevent direct genetic estimates, the accuracy of demographic models is difficult to evaluate. Here we use individual-based, genetically explicit computer simulations in order to investigate the accuracy of two such demographic models aimed at investigating the hierarchical structure of populations. We show that, by and large, these models provide good estimates under a wide range of mating systems and dispersal patterns. However, one of the models should be avoided whenever the focal species' breeding system approaches monogamy with no sex bias in dispersal or when a substructure within social groups is suspected because effective sizes may then be strongly overestimated. The timing during the life cycle at which F-statistics are evaluated is also of crucial importance and attention should be paid to it when designing field sampling since different demographic models assume different timings. Our study shows that individual-based, genetically explicit models provide a promising way of evaluating the accuracy of demographic models of effective size and delineate their field of applicability.     

Small effective population size in the long-toed salamander

The effective population sizes (Ne) of six populations of the long-toed salamander (Ambystoma macrodactylum) from Montana and Idaho, USA were estimated from allozyme data from samples collected in 1978, 1996 and 1997 using the temporal allele frequency method. Five of the six estimates ranged from 23 to 207 (mean = 123 +/- 79); one estimate was indistinguishable from infinity. In order to infer the actual Ne of salamander populations, we compared the frequency distribution of our observed Ne estimates with distributions obtained from simulated populations of known Ne. Our observed Ne estimate distribution was consistent with distributions from simulated populations with Ne values of 10, 25, and 50, suggesting an actual Ne for each of the six salamander populations of less than 100. This Ne estimate agrees with most other Ne estimates for amphibians. We conclude by discussing the conservation implications of small Ne values in amphibians in the context of increasing isolation of populations due to habitat fragmentation.     

Genome size evolution in relation to leaf strategy and metabolic rates revisited

BACKGROUND AND AIMS: It has been proposed that having too much DNA may carry physiological consequences for plants. The strong correlation between DNA content, cell size and cell division rate could lead to predictable morphological variation in plants, including a negative relationship with leaf mass per unit area (LMA). In addition, the possible increased demand for resources in species with high DNA content may have downstream effects on maximal metabolic efficiency, including decreased metabolic rates. METHODS: Tests were made for genome size-dependent variation in LMA and metabolic rates (mass-based photosynthetic rate and dark respiration rate) using our own measurements and data from a plant functional trait database (Glopnet). These associations were tested using two metrics of genome size: bulk DNA amount (2C DNA) and monoploid genome size (1Cx DNA). The data were analysed using an evolutionary framework that included a regression analysis and independent contrasts using a phylogenetic tree with estimates of molecular diversification times. A contribution index for the LMA data set was also calculated to determine which divergences have the greatest influence on the relationship between genome size and LMA. KEY RESULTS AND CONCLUSIONS: A significant negative association was found between bulk DNA amount and LMA in angiosperms. This was primarily a result of influential divergences that may represent early shifts in growth form. However, divergences in bulk DNA amount were positively associated with divergences in LMA, suggesting that the relationship may be indirect and mediated through other traits directly related to genome size. There was a significant negative association between genome size and metabolic rates that was driven by a basal divergence between angiosperms and gymnosperms; no significant independent contrast results were found. Therefore, it is concluded that genome size-dependent constraints acting on metabolic efficiency may not exist within seed plants.     

On the concept of the effective population size

The concept of the effective population size is discussed. It is shown that the “eigenvalue” and the “inbreeding” effective population sizes are in principle different, even though they have been sometimes identified in the literature. On the other hand the “eigenvalue” and “variance” effective sizes are usually both close when the latter exists. Since, however, there are many models for which a variance effective size cannot in principle exist, it seems useful to introduce the eigenvalue effective size and to examine some of its properties.     

Genetic drift and estimation of effective population size

The statistical properties of the standardized variance of gene frequency changes (a quantity equivalent to Wright's inbreeding coefficient) in a random mating population are studied, and new formulae for estimating the effective population size are developed. The accuracy of the formulae depends on the ratio of sample size to effective size, the number of generations involved (t), and the number of loci or alleles used. It is shown that the standardized variance approximately follows the chi(2) distribution unless t is very large, and the confidence interval of the estimate of effective size can be obtained by using this property. Application of the formulae to data from an isolated population of Dacus oleae has shown that the effective size of this population is about one tenth of the minimum census size, though there was a possibility that the procedure of sampling genes was improper.     

The effective population size of some age-structured populations

It was shown in a previous paper that if generations are discrete, then the effective population size of a large population can be derived from the theory of multitype branching processes. It turns out to be proportional to the reciprocal of a term that appears in the denominator of expressions for survival probabilities when there is a supercritical positively regular branching process for which the dominant positive eigenvalue of the first moment matrix is slightly larger than 1. If there is an age-structured population with unchanging proportions among sexes and age groups, then the effective population size is shown to be also obtainable from the theory of multitype branching processes. The expression for this parameter has the same form as in the corresponding model for discrete generations, multiplied by an appropriate measure of the average length of a generation. Results are obtained for dioecious random mating populations, populations reproducing partly by selfing, and populations reproducing partly by full-sib mating.     

Two measures of effective population size for graphs

Effective population size is a key parameter in population ecology because it allows prediction of the dynamics of genetic variation and the rate of genetic drift and inbreeding. It is important for the definition of "nearly neutral" mutations and, hence, has consequences for the fixation or extinction probabilities of advantageous and deleterious mutations. As graph-based population models become increasingly popular for studying evolution in spatially or socially structured populations, a neutral theory for evolution on graphs is called for. Here, we derive formulae for two alternative measures of effective population size, the variance effective and inbreeding effective size of general unweighted and undirected graphs. We show how these two quantities relate to each other and we derive effective sizes for the complete graph the cycle and bipartite graphs. For one-dimensional lattices and small-world graphs, we estimate the inbreeding effective size using simulations. The presented method is suitable for any structured population of haploid individuals with overlapping generations.     

Genome size is negatively correlated with effective population size in ray-finned fish

A recent theory suggesting that genome size and complexity can increase as a passive consequence of small effective population size has generated much controversy. In this article, we demonstrate that freshwater fish species, which have smaller effective population sizes than marine fish species, have larger genomes. We show that genome size is negatively correlated with genetic variability, independent of phylogeny, body size and generation time. Genome duplication is also observed predominantly in freshwater fish. These results suggest that the raw materials of complexity originate under conditions of reduced selection efficiency.     

Variance effective population size is affected by census size in sub-structured populations

Measurement of allele frequency shifts between temporally spaced samples has long been used for assessment of effective population size (N_e), and this ‘temporal method’ provides estimates of N_e referred to as variance effective size (N_eV). We show that N_eV of a local population that belongs to a sub-structured population (a metapopulation) is determined not only by genetic drift and migration rate (m), but also by the census size (N_c). The realized N_eV of a local population can either increase or decrease with increasing m, depending on the relationship between N_e and N_c in isolation. This is shown by explicit mathematical expressions for the factors affecting N_eV derived for an island model of migration. We verify analytical results using high-resolution computer simulations, and show that the phenomenon is not restricted to the island model migration pattern. The effect of N_c on the realized N_eV of a local subpopulation is most pronounced at high migration rates. We show that N_c only affects local N_eV, whereas N_eV for the metapopulation as a whole, inbreeding (N_eI), and linkage disequilibrium (N_eLD) effective size are all independent of N_c. Our results provide a possible explanation to the large variation of N_e/N_c ratios reported in the literature, where N_e is frequently estimated by N_eV. They are also important for the interpretation of empirical N_e estimates in genetic management where local N_eV is often used as a substitute for inbreeding effective size, and we suggest an increased focus on metapopulation N_eV as a proxy for N_eI.     

Selection efficiency and effective population size in Drosophila species

A corollary of the nearly neutral theory of molecular evolution is that the efficiency of natural selection depends on effective population size. In this study, we evaluated the differences in levels of synonymous polymorphism among Drosophila species and showed that these differences can be explained by differences in effective population size. The differences can have implications for the molecular evolution of the Drosophila species, as is suggested by our results showing that the levels of codon bias and the proportion of adaptive substitutions are both higher in species with higher levels of synonymous polymorphism. Moreover, species with lower synonymous polymorphism have higher levels of nonsynonymous polymorphism and larger content of repetitive sequences in their genomes, suggesting a diminished efficiency of selection in species with smaller effective population size.