Contrasting patterns of polymorphism and divergence on the Z chromosome and autosomes in two Ficedula flycatcher species

In geographic areas where pied and collared flycatchers (Ficedula hypoleuca and F. albicollis) breed in sympatry, hybridization occurs, leading to gene flow (introgression) between the two recently diverged species. Notably, while such introgression is observable at autosomal loci it is apparently absent at the Z chromosome, suggesting an important role for genes on the Z chromosome in creating reproductive isolation during speciation. To further understand the role of Z-linked loci in the formation of new species, we studied genetic variation of the two species from regions where they live in allopatry. We analyzed patterns of polymorphism and divergence in introns from 9 Z-linked and 23 autosomal genes in pied and collared flycatcher males. Average variation on the Z chromosome is greatly reduced compared to neutral expectations based on autosomal diversity in both species. We also observe significant heterogeneity between patterns of polymorphism and divergence at Z-linked loci and a relative absence of polymorphisms that are shared by the two species on the Z chromosome compared to the autosomes. We suggest that these observations may indicate the action of recurrent selective sweeps on the Z chromosome during the evolution of the two species, which may be caused by sexual selection acting on Z-linked genes. Alternatively, reduced variation on the Z chromosome could result from substantially higher levels of introgression at autosomal than at Z-linked loci or from a complex demographic history, such as a population bottleneck.     

gesp: A computer program for modelling genetic effective population size,inbreeding and divergence in substructured populations

The genetically effective population size (N_e) is of key importance for quantifying rates of inbreeding and genetic drift and is often used in conservation management to set targets for genetic viability. The concept was developed for single, isolated populations and the mathematical means for analysing the expected N_e in complex, subdivided populations have previously not been available. We recently developed such analytical theory and central parts of that work have now been incorporated into a freely available software tool presented here. gesp (Genetic Effective population size, inbreeding and divergence in Substructured Populations) is R‐based and designed to model short‐ and long‐term patterns of genetic differentiation and effective population size of subdivided populations. The algorithms performed by gesp allow exact computation of global and local inbreeding and eigenvalue effective population size, predictions of genetic divergence among populations (G_ST) as well as departures from random mating (F_IS, F_IT) while varying (i) subpopulation census and effective size, separately or including trend of the global population size, (ii) rate and direction of migration between all pairs of subpopulations, (iii) degree of relatedness and divergence among subpopulations, (iv) ploidy (haploid or diploid) and (v) degree of selfing. Here, we describe gesp and exemplify its use in conservation genetics modelling.     

Antagonistic selection factors induce a continuous population divergence in a polymorphism

Understanding the relative importance of selection and stochastic factors in population divergence of adaptive traits is a classical topic in evolutionary biology. However, it is difficult to separate these factors and detect the effects of selection when two or more contrasting selective factors are simultaneously acting on a single locus. In the damselfly Ischnura senegalensis, females exhibit color dimorphism and morph frequencies change geographically. We here evaluated the role of selection and stochastic factors in population divergence of morph frequencies by comparing the divergences in color locus and neutral loci. Comparisons between population pairwise F_ST for neutral loci and for the color locus did not detect any stochastic factors affecting color locus. Although comparison between population divergence in color and neutral loci using all populations detected only divergent selection, we detected two antagonistic selective factors acting on the color locus, that is, balancing and divergent selection, when considering geographical distance between populations. Our results suggest that a combination of two antagonistic selective factors, rather than stochastic factors, establishes the geographic cline in morph frequency in this system.     

Longevity is associated with relative brain size in birds

Brain size of vertebrates has long been recognized to evolve in close association with basic life‐history traits, including lifespan. According to the cognitive buffer hypothesis, large brains facilitate the construction of behavioral responses against novel socioecological challenges through general cognitive processes, which should reduce mortality and increase lifespan. While the occurrence of brain size–lifespan correlation has been well documented in mammals, much less evidence exists for a robust link between brain size and longevity in birds. The aim of this study was to use phylogenetically controlled comparative approach to test for the relationship between brain size and longevity among 384 avian species from 23 orders. We used maximum lifespan and maximum reproductive lifespan as the measures of longevity and accounted for a set of possible confounding effects, such as allometry, sampling effort, geographic patterns, and life‐history components (clutch size, incubation length, and mode of development). We found that both measures of longevity positively correlated with relative (residual) brain size. We also showed that major diversification of brain size preceded diversification of longevity in avian evolution. In contrast to previous findings, the effect of brain size on longevity was consistent across lineages with different development patterns, although the relatively low strength of this correlation could likely be attributed to the ubiquity of allomaternal care associated with the altricial mode of development. Our study indicates that the positive relationship between brain size and longevity in birds may be more general than previously thought.     

Karyotypic polymorphism of the zebra finch Z chromosome

We describe a karyotypic polymorphism on the zebra finch Z chromosome. This polymorphism was discovered because of a difference in the position of the centromere and because it occurs at varying frequencies in domesticated colonies in the USA and Germany and among two zebra finch subspecies. Using DNA fluorescent in situ hybridization to map specific Z genes and measurements of DNA replication, we show that this polymorphism is the result of a large pericentric inversion involving the majority of the chromosome. We sequenced a likely breakpoint for the inversion and found many repetitive sequences. Around the breakpoint, there are numerous repetitive sequences and several copies of PAK3 (p21-activated kinase 3)-related sequences (PAK3Z) which showed testes-specific expression by RT-PCR. Our findings further suggest that the sequenced genome of the zebra finch may be derived from a male heterozygote for the Z chromosome polymorphism. This finding, in combination with regional differences in the frequency of the polymorphism, has important consequences for future studies using zebra finches.     

Estimating divergence time and ancestral effective population size of Bornean and Sumatran orangutan subspecies using a coalescent hidden Markov model

Due to genetic variation in the ancestor of two populations or two species, the divergence time for DNA sequences from two populations is variable along the genome. Within genomic segments all bases will share the same divergence-because they share a most recent common ancestor-when no recombination event has occurred to split them apart. The size of these segments of constant divergence depends on the recombination rate, but also on the speciation time, the effective population size of the ancestral population, as well as demographic effects and selection. Thus, inference of these parameters may be possible if we can decode the divergence times along a genomic alignment. Here, we present a new hidden Markov model that infers the changing divergence (coalescence) times along the genome alignment using a coalescent framework, in order to estimate the speciation time, the recombination rate, and the ancestral effective population size. The model is efficient enough to allow inference on whole-genome data sets. We first investigate the power and consistency of the model with coalescent simulations and then apply it to the whole-genome sequences of the two orangutan sub-species, Bornean (P. p. pygmaeus) and Sumatran (P. p. abelii) orangutans from the Orangutan Genome Project. We estimate the speciation time between the two sub-species to be thousand years ago and the effective population size of the ancestral orangutan species to be , consistent with recent results based on smaller data sets. We also report a negative correlation between chromosome size and ancestral effective population size, which we interpret as a signature of recombination increasing the efficacy of selection.     

Low effective population size and survivorship in a grassland grouse

Assessments of census size (N _c) and effective population size (N _e) are necessary for the conservation of species exhibiting population declines. We examined two populations (Oklahoma and New Mexico) of the lesser prairie-chicken (Tympanuchus pallidicinctus), a declining lek-breeding bird, in which one population (Oklahoma) has larger clutch size and more nesting attempts per year but lower survival caused by human changes to the landscape. We estimated demographic and genetic estimates of N _e for each population and found that both populations have low N _e estimates with a risk of inbreeding depression. Although Oklahoma females produce a larger number of offspring, the proportion of females successfully reproducing is not higher than in New Mexico. Higher reproductive effort has likely reached a physiological limit in Oklahoma prairie-chickens but has not led to a higher N _e or even a larger N _c than New Mexico. We propose that future conservation efforts focus on maximizing survivorship and decreasing the variance in reproductive success because these factors are more likely than increasing reproductive output alone to yield population persistence in lek-breeding species.     

The influence of stochastic and selective forces in the population divergence of female colour polymorphism in damselflies of the genus Ischnura

Disentangling the relative importance and potential interactions of selection and genetic drift in driving phenotypic divergence of species is a classical research topic in population genetics and evolutionary biology. Here, we evaluate the role of stochastic and selective forces on population divergence of a colour polymorphism in seven damselfly species of the genus Ischnura, with a particular focus on I. elegans and I. graellsii. Colour-morph frequencies in Spanish I. elegans populations varied greatly, even at a local scale, whereas more similar frequencies were found among populations in eastern Europe. In contrast, I. graellsii and the other five Ischnura species showed little variation in colour-morph frequencies between populations. F(ST)-outlier analyses revealed that the colour locus deviated strongly from neutral expectations in Spanish populations of I. elegans, contrasting the pattern found in eastern European populations, and in I. graellsii, where no such discrepancy between morph divergence and neutral divergence could be detected. This suggests that divergent selection has been operating on the colour locus in Spanish populations of I. elegans, whereas processes such as genetic drift, possibly in combination with other forms of selection (such as negative frequency-dependent selection), appear to have been present in other regions, such as eastern Europe. Overall, the results indicate that both selective and stochastic processes operate on these colour polymorphisms, and suggest that the relative importance of factors varies between geographical regions.     

Volatility in the effective size of a freshwater gastropod population

Despite the utility of gastropod models for the study of evolutionary processes of great generality and importance, their effective population size has rarely been estimated in the field. Here, we report allele frequency variance at three allozyme‐encoding loci monitored over 7 years in a population of the invasive freshwater pulmonate snail Physa acuta (Draparnaud 1805), estimating effective population size with both single‐sample and two‐sample approaches. Estimated N_e declined from effectively infinite in 2009 to approximately 40–50 in 2012 and then rose back to infinity in 2015, corresponding to a striking fluctuation in the apparent census size of the population. Such volatility in N_e may reflect cryptic population subdivision.     

Genetic diversity, population structure, effective population size and demographic history of the Finnish wolf population

The Finnish wolf population (Canis lupus) was sampled during three different periods (1996-1998, 1999-2001 and 2002-2004), and 118 individuals were genotyped with 10 microsatellite markers. Large genetic variation was found in the population despite a recent demographic bottleneck. No spatial population subdivision was found even though a significant negative relationship between genetic relatedness and geographic distance suggested isolation by distance. Very few individuals did not belong to the local wolf population as determined by assignment analyses, suggesting a low level of immigration in the population. We used the temporal approach and several statistical methods to estimate the variance effective size of the population. All methods gave similar estimates of effective population size, approximately 40 wolves. These estimates were slightly larger than the estimated census size of breeding individuals. A Bayesian model based on Markov chain Monte Carlo simulations indicated strong evidence for a long-term population decline. These results suggest that the contemporary wolf population size is roughly 8% of its historical size, and that the population decline dates back to late 19th century or early 20th century. Despite an increase of over 50% in the census size of the population during the whole study period, there was only weak evidence that the effective population size during the last period was higher than during the first. This may be caused by increased inbreeding, diminished dispersal within the population, and decreased immigration to the population during the last study period.     

The effective population size of an age-structured population with a sex-linked locus

Let a population have the same age distribution and age-specific sex ratios at times 0, 1, 2,..., and let M, F, and L, respectively, be the numbers of males and females in the youngest age group and the generation interval. It can then be shown that if there is a sex-linked locus the fixation probabilities of a neutral allele are respectively 1/3LM or 1/3LF if the allele first appears in one newborn male or in one newborn female. The effective population size can then be derived. It is the same as for a population with discrete generations having the same means, variances, and covariances of male and female progeny during a lifetime and the same number of individuals entering the population per generation.     

Partial migration in birds: tests of three hypotheses in a tropical lekking frugivore

1. Partially migratory species provide opportunities to understand which ecological factors cause some animals to migrate when others remain resident year round. Partial migration in birds has been explained by the dominance, arrival-time, and body-size hypotheses. 2. Testing these hypotheses has proven difficult due to the similarities of the predictions they make in temperate-breeding long-distance migrants. In tropical altitudinal migrants, however, these hypotheses make different predictions regarding the sex, age, and condition of migrants and residents. 3. Among white-ruffed manakins in Costa Rica, young birds were not more likely to migrate (as predicted by the dominance hypothesis), nor were females more likely to migrate (as predicted by the arrival-time hypothesis). All condition-related variables interacted with sex, together explaining much of the variation in migratory behaviour. 4. I re-articulate the body-size hypothesis in the context of tropical altitudinal bird migration, focusing explicitly on how limited foraging opportunities and differences in individual condition affect fasting ability during torrential rains. Despite ample food, the smallest birds or those stressed by parasites or moult may risk starvation at breeding elevations due to a reduction in foraging time. These results highlight how intrinsic and extrinsic factors may interact to produce observed patterns of within- and among-species variation in migratory behaviour.     

Coalescent process with fluctuating population size and its effective size

We consider a Wright-Fisher model whose population size is a finite Markov chain. We introduce a sequence of two-dimensional discrete time Markov chains whose components describe the coalescent process and the fluctuation of population size. For the limiting process of the sequence of Markov chains, the relationship of the expectation of coalescence time to the harmonic and the arithmetic means of population sizes is shown, and the Laplace transform of the distribution of coalescence time is calculated. We define the coalescence effective population size (cEPS) by the expectation of coalescence time. We show that cEPS is strictly larger (resp. smaller) than the harmonic (resp. arithmetic) mean. As the population size fluctuates more quickly (resp. slowly), cEPS is closer to the harmonic (resp. arithmetic) mean. For the case of a two-valued Markov chain, we show the explicit expression of cEPS and its dependency on the sample size.     

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.     

Genetic variation in a semi-natural Drosophila population after a bottleneck I. Lethals,their allelism and effective population size

A semi-natural Drosophila melanogaster population was twice forced through a genetic bottleneck and allowed to recover naturally. In one case additional variation was introduced to the recovering population. The percentage of lethal chromosomes, the level of allelism between these lethals, and the effective population size calculated from the allelism of these lethals all rose sharply in the few generations following each bottleneck, though this was not the case in the very first generation. Thereafter this rise decelerated rapidly and never returned to pre-bottleneck levels. Additional introduced variation had little effect. The reasons for and implications of this pattern have been considered.     

Effects of population size and metapopulation dynamics on a mating-system polymorphism

The evolutionary dynamics of neutral alleles under the Wright-Fisher model are well understood. Similarly, the effect of population turnover on neutral genetic diversity in a metapopulation has attracted recent attention in theoretical studies. Here we present the results of computer simulations of a simple model that considers the effects of finite population size and metapopulation dynamics on a mating-system polymorphism involving selfing and outcrossing morphs. The details of the model are based on empirical data from dimorphic populations of the annual plant Eichhornia paniculata, but the results are also of relevance to species with density-dependent selfing rates in general. In our model, the prior selfing rate is determined by two alleles segregating at a single diploid locus. After prior selfing occurs, some remaining ovules are selfed through competing self-fertilisation in finite populations as a result of random mating among gametes. Fitness differences between the mating-system morphs were determined by inbreeding depression and pollen discounting in a context-dependent manner. Simulation results showed evidence of frequency dependence in the action of pollen discounting and inbreeding depression in finite populations. In particular, as a result of selfing in outcrossers through random mating among gametes, selfers experienced a "fixation bias" through drift, even when the mating-system locus was selectively neutral. In a metapopulation, high colony turnover generally favoured the fixation of the outcrossing morph, because inbreeding depression reduced opportunities for colony establishment by selfers through seed dispersal. Our results thus demonstrate that population size and metapopulation processes can lead to evolutionary dynamics involving pollen and seed dispersal that are not predicted for large populations with stable demography.