From individual behavior to metapopulation dynamics: unifying the patchy population and classic metapopulation models

Spatially structured populations in patchy habitats show much variation in migration rate, from patchy populations in which individuals move repeatedly among habitat patches to classic metapopulations with infrequent migration among discrete populations. To establish a common framework for population dynamics in patchy habitats, we describe an individual-based model (IBM) involving a diffusion approximation of correlated random walk of individual movements. As an example, we apply the model to the Glanville fritillary butterfly (Melitaea cinxia) inhabiting a highly fragmented landscape. We derive stochastic patch occupancy model (SPOM) approximations for the IBMs assuming pure demographic stochasticity, uncorrelated environmental stochasticity, or completely correlated environmental stochasticity in local dynamics. Using realistic parameter values for the Glanville fritillary, we show that the SPOMs mimic the behavior of the IBMs well. The SPOMs derived from IBMs have parameters that relate directly to the life history and behavior of individuals, which is an advantage for model interpretation and parameter estimation. The modeling approach that we describe here provides a unified framework for patchy populations with much movements among habitat patches and classic metapopulations with infrequent movements.     

Sex-specific genetic structure and social organization in Central Asia: insights from a multi-locus study

In the last two decades, mitochondrial DNA (mtDNA) and the non-recombining portion of the Y chromosome (NRY) have been extensively used in order to measure the maternally and paternally inherited genetic structure of human populations, and to infer sex-specific demography and history. Most studies converge towards the notion that among populations, women are genetically less structured than men. This has been mainly explained by a higher migration rate of women, due to patrilocality, a tendency for men to stay in their birthplace while women move to their husband's house. Yet, since population differentiation depends upon the product of the effective number of individuals within each deme and the migration rate among demes, differences in male and female effective numbers and sex-biased dispersal have confounding effects on the comparison of genetic structure as measured by uniparentally inherited markers. In this study, we develop a new multi-locus approach to analyze jointly autosomal and X-linked markers in order to aid the understanding of sex-specific contributions to population differentiation. We show that in patrilineal herder groups of Central Asia, in contrast to bilineal agriculturalists, the effective number of women is higher than that of men. We interpret this result, which could not be obtained by the analysis of mtDNA and NRY alone, as the consequence of the social organization of patrilineal populations, in which genetically related men (but not women) tend to cluster together. This study suggests that differences in sex-specific migration rates may not be the only cause of contrasting male and female differentiation in humans, and that differences in effective numbers do matter.     

Sequential Markov coalescent algorithms for population models with demographic structure

We analyse sequential Markov coalescent algorithms for populations with demographic structure: for a bottleneck model, a population-divergence model, and for a two-island model with migration. The sequential Markov coalescent method is an approximation to the coalescent suggested by McVean and Cardin, and by Marjoram and Wall. Within this algorithm we compute, for two individuals randomly sampled from the population, the correlation between times to the most recent common ancestor and the linkage probability corresponding to two different loci with recombination rate R between them. These quantities characterise the linkage between the two loci in question. We find that the sequential Markov coalescent method approximates the coalescent well in general in models with demographic structure. An exception is the case where individuals are sampled from populations separated by reduced gene flow. In this situation, the correlations may be significantly underestimated. We explain why this is the case.     

Combined next‐generation sequencing and morphology reveal fine‐scale speciation in Crocodile Skinks (Squamata: Scincidae: Tribolonotus)

Next‐generation sequencing has vast potential to revolutionize the fields of phylogenetics and population genetics through its ability to collect genomic scale data sets of thousands of orthologous loci. Despite this potential, other types of data (e.g. morphology, ecology) remain important, particularly for studies endeavouring to delimit species. Here, we integrate next‐generation sequencing with morphology to examine divergence between populations of Tribolonotus pseudoponceleti on the islands of Buka and Bougainville in the Solomon Archipelago. We used the Ion Torrent PGM to collect over 648 Mbp of sequence data for 12 samples, representing 1526 loci recovered from all samples, and 3342 were recovered from at least six samples. Genetic structure analyses strongly support the distinctiveness of these two populations, and Bayes factor delimitations decisively select speciation between Buka and Bougainville. Principal components and discriminant function analyses reveal concordant morphological divergence. Finally, demographic analyses via diffusion approximation and approximate Bayesian computation prefer a complex model of mid‐Pleistocene divergence with migration, and a later decrease or cessation of migration and population size shift, suggesting a scenario in which migration was enabled by Pleistocene merging of these two islands, and limited when isolated by higher sea levels. Further analysis of four Sanger sequenced loci in IMa2 had limited power to distinguish among models including and excluding migration, but resulted in similar population size and divergence time estimates, although with much broader confidence intervals. This study represents a framework for how next‐generation sequencing and morphological data can be combined and leveraged towards validating putative species and testing demographic scenarios for speciation.     

Accipiter hawks of the Laurentian Upland and the Interior Plains undertake the longest migrations: insights from birds banded or recovered in Veracruz,Mexico

Bird banding has allowed us to understand diverse aspects of the life histories of migratory raptors. However, most banding stations are located at northern latitudes so what we know about the movements of these raptors is biased toward higher latitudes, primarily from Canada and the United States, leaving important gaps in our knowledge of their movements at lower latitudes. Our objective was to describe the migratory movements of Sharp-shinned (Accipiter striatus) and Cooper’s (A. cooperii) hawks based on banding and recapture records of birds that migrate through Veracruz, Mexico. More specifically, we sought to determine their breeding, migration, and non-breeding locations, estimate their migration distances, and contribute to a better understanding of their migration patterns. With a total of 80 records, we calculated migration distances and used Kernel Density Estimation analyses to identify where these hawks were recaptured or recovered by season. The distribution of recaptures and recoveries largely coincided with breeding locations in the Laurentian Upland and the Interior Plains physiographic regions. All migration records follow a trajectory that extends from the midwestern United States to the Gulf coastal plain of Mexico. The mean breeding season migration distance to Veracruz was 3374 km (a difference of 27 degrees of latitude) for Sharp-shinned Hawks and 2926 km (a difference of 25 degrees of latitude) for Cooper’s Hawks. Our non-breeding records indicate that populations of Accipiter hawks from these North American populations migrate the longest distances to reach Central America, the southernmost distribution of their migratory populations. Distances covered by both species represent round-trip migrations that may be as long as 10,000 km. Our results support those of previous studies and illustrate how continental physiography influences the migration routes, migratory behavior, and migratory connectivity of these hawks.     

Sex‐biased migration in humans: what should we expect from genetic data?

Different patterns of mitochondrial and Y-chromosome diversity have been cited as evidence of long-term patrilocality in human populations. However, what patterns are expected depends on the nature of the sampling scheme. Samples from a local region reveal only the recent demographic history of that region, whereas sampling over larger geographic scales accesses older demographic processes. A historical change in migration becomes evident first at local geographic scales, and alters global patterns of genetic diversity only after sufficient time has passed. Analysis of forager populations in the ethnographic record suggests that patrilocality may not have predominated among pre-agricultural humans. The higher female migration rate inferred by some genetic studies may reflect a shift to patrilocality in association with the emergence of agriculture. A recent global survey does not show the expected effects of higher female migration, possibly because the sampling scheme used for this study is accessing pre-agricultural human migration patterns. In this paper, we show how the demographic shift associated with agriculture might affect genetic diversity over different spatial scales. We also consider the prospects for studying sex-biased migration using the X-linked and autosomal markers. These multi-locus comparisons have the potential of providing more robust estimates of sex differences than Y-linked and mitochondrial data, but only if a very large number of loci are included in the analysis.     

Migration in butterflies: a global overview

Insect populations including butterflies are declining worldwide, and they are becoming an urgent conservation priority in many regions. Understanding which butterfly species migrate is critical to planning for their conservation, because management actions for migrants need to be coordinated across time and space. Yet, while migration appears to be widespread among butterflies, its prevalence, as well as its taxonomic and geographic distribution are poorly understood. The study of insect migration is hampered by their small size and the difficulty of tracking individuals over long distances. Here we review the literature on migration in butterflies, one of the best-known insect groups. We find that nearly 600 butterfly species show evidence of migratory movements. Indeed, the rate of ‘discovery’ of migratory movements in butterflies suggests that many more species might in fact be migratory. Butterfly migration occurs across all families, in tropical as well as temperate taxa; Nymphalidae has more migratory species than any other family (275 species), and Pieridae has the highest proportion of migrants (13%; 133 species). Some 13 lines of evidence have been used to ascribe migration status in the literature, but only a single line of evidence is available for 92% of the migratory species identified, with four or more lines of evidence available for only 10 species – all from the Pieridae and Nymphalidae. Migratory butterflies occur worldwide, although the geographic distribution of migration in butterflies is poorly resolved, with most data so far coming from Europe, USA, and Australia. Migration is much more widespread in butterflies than previously realised – extending far beyond the well-known examples of the monarch Danaus plexippus and the painted lady Vanessa cardui – and actions to conserve butterflies and insects in general must account for the spatial dependencies introduced by migratory movements.     

The dynamics of transposable elements in structured populations

We analyzed the dynamics of transposable elements (TEs) according to Wright's island and continent-island models, assuming that selection tends to counter the deleterious effects of TEs. We showed that migration between host populations has no impact on either the existence or the stability of the TE copy number equilibrium points obtained in the absence of migration. However, if the migration rate is slower than the transposition rate or if selection is weak, then the TE copy numbers in all the populations can be expected to slowly become homogeneous, whereas a heterogeneous TE copy number distribution between populations is maintained if TEs are mobilized in some populations. The mean TE copy number is highly sensitive to the population size, but as a result of migration between populations, it decreases as the sum of the population sizes increases and tends to reach the same value in these populations. We have demonstrated the existence of repulsion between TE insertion sites, which is established by selection and amplified by drift. This repulsion is reduced as much as the migration rate is higher than the recombination rate between the TE insertion sites. Migration and demographic history are therefore strong forces in determining the dynamics of TEs within the genomes and the populations of a species.     

Migration of wild and captive‐bred Little Bustards Tetrax tetrax: releasing birds from Spain threatens attempts to conserve declining French populations

Populations of the Little Bustard Tetrax tetrax in the farmlands of Europe have declined greatly over the last century. In Western Europe, France now holds the only remaining migratory population, which currently numbers fewer than 300 displaying males. However, the movements of these birds are virtually unknown, in spite of the important implications of this information for the conservation of this species. We identified migratory movements and overwintering areas of French migratory populations, using wild individuals fitted with satellite or radio‐transmitters. Little Bustards completed their migration journey over a relatively short time period (2–5 days), with nocturnal migration flights of 400–600 km per night. All birds overwintered in Iberia. In addition, we tested the consequences of captive rearing on migratory movements. French wild adults and French captive‐bred juveniles behaved similarly with regard to migration, suggesting that hand‐raising does not alter migratory movements. However, birds originating from eggs collected in Spain and reared in western France did not migrate, suggesting a genetic component to migratory behaviour. These results therefore suggest that a conservation strategy involving the release in France of birds hatched from eggs collected in Spain may imperil the expression of migratory movements of the French population. More generally, to maintain the integrity of native populations, the introduced individuals should mimic their migratory movements and behaviour.     

Y-chromosome analysis confirms highly sex-biased dispersal and suggests a low male effective population size in bonobos (Pan paniscus)

Dispersal is a rare event that is difficult to observe in slowly maturing, long-lived wild animal species such as the bonobo. In this study we used sex-linked (mitochondrial DNA sequence and Y-chromosome microsatellite) markers from the same set of individuals to estimate the magnitude of difference in effective dispersal between the sexes and to investigate the long-term demographic history of bonobos. We sampled 34 males from four distinct geographical areas across the bonobo distribution range. As predicted for a female-dispersing species, we found much higher levels of differentiation among local bonobo populations based upon Y-chromosomal than mtDNA genetic variation. Specifically, almost all of the Y-chromosomal variation distinguished populations, while nearly all of the mtDNA variation was shared between populations. Furthermore, genetic distance correlated with geographical distance for mtDNA but not for the Y chromosome. Female bonobos have a much higher migration rate and/or effective population size as compared to males, and the estimate for the mitochondrial TMRCA (time to most recent common ancestor) was approximately 10 times greater than the estimate for the Y chromosome (410,000 vs. 40,000-45,000). For humans the difference is merely a factor of two, suggesting a more stable demographic history in bonobos in comparison to humans.     

Evaluating the performance of a multilocus Bayesian method for the estimation of migration rates

Bayesian methods have become extremely popular in molecular ecology studies because they allow us to estimate demographic parameters of complex demographic scenarios using genetic data. Articles presenting new methods generally include sensitivity studies that evaluate their performance, but they tend to be limited and need to be followed by a more thorough evaluation. Here we evaluate the performance of a recent method, bayesass , which allows the estimation of recent migration rates among populations, as well as the inbreeding coefficient of each local population. We expand the simulation study of the original publication by considering multi-allelic markers and scenarios with varying number of populations. We also investigate the effect of varying migration rates and F _ST more thoroughly in order to identify the region of parameter space where the method is and is not able to provide accurate estimates of migration rate. Results indicate that if the demographic history of the species being studied fits the assumptions of the inference model, and if genetic differentiation is not too low ( F _ST ≥ 0.05), then the method can give fairly accurate estimates of migration rates even when they are fairly high (about 0.1). However, when the assumptions of the inference model are violated, accurate estimates are obtained only if migration rates are very low ( m  = 0.01) and genetic differentiation is high ( F _ST ≥ 0.10). Our results also show that using posterior assignment probabilities as an indication of how much confidence we can place on the assignments is problematical since the posterior probability of assignment can be very high even when the individual assignments are very inaccurate.     

Migration rates, frequency-dependent selection and the self-incompatibility locus in Leavenworthia (brassicaceae)

Loci subject to negative frequency-dependent selection are expected to exhibit higher effective migration rates compared to reference loci. Although the number of gene copies transferred between populations by migration is the same for all genes, those subject to negative frequency-dependent selection are more likely to be retained in the immigrant population because rare alleles are selectively favored. So far, evidence for this prediction has been indirect, based on summary statistics rather than on migration rate estimates. Here, we introduce an approximate Bayesian procedure to jointly estimate migration rates at two predefined sets of loci between two populations. We applied the procedure to compare migration rate estimates at the self-incompatibility locus (S-locus) with that at 10 reference loci in two plant species, Leavenworthia alabamica and L. crassa (Brassicaceae). The maximum likelihood estimate for the proportion of migrants (m) was four times higher at the S-locus than at reference loci, but the difference was not statistically significant. Lack of significance might be due to insufficient data, but perhaps also to the recent divergence of the two species (311 ka), because we also show using simulations that the effective migration rate at the S-locus is expected to increase with increasing divergence time. These findings aid in understanding the evolutionary dynamics of negative frequency-dependent selection and they suggest that divergence time should be accounted for when employing migration rates to help detect negative frequency-dependent selection.     

Holding steady: Little change in intensity or timing of bird migration over the Gulf of Mexico

Quantifying the timing and intensity of migratory movements is imperative for understanding impacts of changing landscapes and climates on migratory bird populations. Billions of birds migrate in the Western Hemisphere, but accurately estimating the population size of one migratory species, let alone hundreds, presents numerous obstacles. Here, we quantify the timing, intensity, and distribution of bird migration through one of the largest migration corridors in the Western Hemisphere, the Gulf of Mexico (the Gulf). We further assess whether there have been changes in migration timing or intensity through the Gulf. To achieve this, we integrate citizen science (eBird) observations with 21 years of weather surveillance radar data (1995–2015). We predicted no change in migration timing and a decline in migration intensity across the time series. We estimate that an average of 2.1 billion birds pass through this region each spring en route to Nearctic breeding grounds. Annually, half of these individuals pass through the region in just 18 days, between April 19 and May 7. The western region of the Gulf showed a mean rate of passage 5.4 times higher than the central and eastern regions. We did not detect an overall change in the annual numbers of migrants (2007–2015) or the annual timing of peak migration (1995–2015). However, we found that the earliest seasonal movements through the region occurred significantly earlier over time (1.6 days decade^?1). Additionally, body mass and migration distance explained the magnitude of phenological changes, with the most rapid advances occurring with an assemblage of larger‐bodied shorter‐distance migrants. Our results provide baseline information that can be used to advance our understanding of the developing implications of climate change, urbanization, and energy development for migratory bird populations in North America.     

Nucleotide variation at Msn and Alas2, two genes flanking the centromere of the X chromosome in humans

The centromeric region of the X chromosome in humans experiences low rates of recombination over a considerable physical distance. In such a region, the effects of selection may extend to linked sites that are far away. To investigate the effects of this recombinational environment on patterns of nucleotide variability, we sequenced 4581 bp at Msn and 4697 bp at Alas2, two genes situated on either side of the X chromosome centromere, in a worldwide sample of 41 men, as well as in one common chimpanzee and one orangutan. To investigate patterns of linkage disequilibrium (LD) across the centromere, we also genotyped several informative sites from each gene in 120 men from sub-Saharan Africa. By studying X-linked loci in males, we were able to recover haplotypes and study long-range patterns of LD directly. Overall patterns of variability were remarkably similar at these two loci. Both loci exhibited (i) very low levels of nucleotide diversity (among the lowest seen in the human genome); (ii) a strong skew in the distribution of allele frequencies, with an excess of both very-low and very-high-frequency derived alleles in non-African populations; (iii) much less variation in the non-African than in the African samples; (iv) very high levels of population differentiation; and (v) complete LD among all sites within loci. We also observed significant LD between Msn and Alas2 in Africa, despite the fact that they are separated by approximately 10 Mb. These observations are difficult to reconcile with a simple demographic model but may be consistent with positive and/or purifying selection acting on loci within this large region of low recombination.     

Social transmission of migratory knowledge: quantifying the risk of losing migratory behavior

When migration is a learned behavior, small populations have a significant problem of maintaining migratory knowledge across generations. These populations risk losing migratory behavior entirely, which may exacerbate existing stressors on population size. Here we investigated the success of various behavioral, demographic, and social factors towards maintaining migration within small populations. Using a discrete-time probabilistic model to simulate repeated migrations, we found that migratory group size plays an important role in maintaining migratory knowledge within the population. Rare, large groups allow for migratory knowledge to be spread to many individuals at once. When a population learns migration information incrementally, the presence of individuals that can learn quickly, therefore transitioning rapidly into leaders, has a profound impact on migrational persistence. Furthermore, small populations are better able to maintain migratory behavior when groups rely on informed leaders as compared to using collective group knowledge, even when that collective knowledge is heavily weighted towards knowledgeable individuals. Finally, we found that both species with short lifespans and species that migrate with fixed group compositions are at especially high risk of losing their migration behavior at small population sizes.     

Imbalanced segregation of recombinant haplotypes in hybrid populations reveals inter- and intrachromosomal Dobzhansky-Muller incompatibilities

Dobzhansky-Muller incompatibilities (DMIs) are a major component of reproductive isolation between species. DMIs imply negative epistasis and are exposed when two diverged populations hybridize. Mapping the locations of DMIs has largely relied on classical genetic mapping. Approaches to date are hampered by low power and the challenge of identifying DMI loci on the same chromosome, because strong initial linkage of parental haplotypes weakens statistical tests. Here, we propose new statistics to infer negative epistasis from haplotype frequencies in hybrid populations. When two divergent populations hybridize, the variance in heterozygosity at two loci decreases faster with time at DMI loci than at random pairs of loci. When two populations hybridize at near-even admixture proportions, the deviation of the observed variance from its expectation becomes negative for the DMI pair. This negative deviation enables us to detect intermediate to strong negative epistasis both within and between chromosomes. In practice, the detection window in hybrid populations depends on the demographic scenario, the recombination rate, and the strength of epistasis. When the initial proportion of the two parental populations is uneven, only strong DMIs can be detected with our method unless migration prevents parental haplotypes from being lost. We use the new statistics to infer candidate DMIs from three hybrid populations of swordtail fish. We identify numerous new DMI candidates, some of which are inferred to interact with several loci within and between chromosomes. Moreover, we discuss our results in the context of an expected enrichment in intrachromosomal over interchromosomal DMIs.     

Migration distance rather than migration rate explains genetic diversity in human patrilocal groups

In patrilocal groups, females preferentially move to join their mate’s paternal relatives. The gender‐biased gene flow generated by this cultural practice is expected to affect genetic diversity across human populations. Greater female than male migration is predicted to result in a larger decrease in between‐group differentiation for mitochondrial DNA (mtDNA) than for the non‐recombining part of the Y chromosome (NRY). We address the question of how patrilocality affects the distribution of genetic variation in human populations controlling for confounding factors such as ethno‐linguistic heterogeneity and geographic distance which possibly explain the contradictory results observed in previous studies. By combining genetic and bio‐demographic data from Lesotho and Spain, we show that preferential female migration over short distances appears to minimize the impact of a generally higher female migration rate in patrilocal communities, suggesting patrilocality might influence genetic variation only at short ranges.     

Population structure and gene flow among anadromous arctic lamprey (Lethenteron camtschaticum) populations deduced from polymorphic microsatellite loci

Information on migration ecology is important for effective conservation and management of fishery resources, particularly diadromous animals. We investigated the genetic population structure and gene flow pattern of anadromous Arctic lamprey Lethenteron camtschaticum by analyzing polymorphic microsatellite loci. Bayesian population structure analysis was used to estimate the existence of two genetically divergent ancestral sources and latitudinal gradual changes of their frequencies among the present populations. When hypotheses of historical migration models were tested using coalescent-based methods, the best model was found to be an n-island model assuming equal population size and reciprocal migration among all populations. These results suggest that L. camtschaticum has considerable ability to migrate long distances in the sea and has lower homing abilities. For resource management of L. camtschaticum, unconstrained gene flow across all populations should be maintained. The present findings might be beneficial for conservation and contribute the sustainable use of L. camtschaticum resource.     

Inferring recent migration rates from individual genotypes

We present a novel and straightforward method for estimating recent migration rates between discrete populations using multilocus genotype data. The approach builds upon a two-step sampling design, where individual genotypes are sampled before and after dispersal. We develop a model that estimates all pairwise backwards migration rates ( m_ij , the probability that an individual sampled in population i is a migrant from population j ) between a set of populations. The method is validated with simulated data and compared with the methods of BayesAss and Structure. First, we use data for an island model and then we consider more realistic data simulations for a metapopulation of the greater white-toothed shrew ( Crocidura russula ). We show that the precision and bias of estimates primarily depend upon the proportion of individuals sampled in each population. Weak sampling designs may particularly affect the quality of the coverage provided by 95% highest posterior density intervals. We further show that it is relatively insensitive to the number of loci sampled and the overall strength of genetic structure. The method can easily be extended and makes fewer assumptions about the underlying demographic and genetic processes than currently available methods. It allows backwards migration rates to be estimated across a wide range of realistic conditions.