Modelling climate‐change‐induced nonlinear thresholds in cephalopod population dynamics

A significant global challenge lies in our current inability to anticipate, and therefore prepare for, critical ecological thresholds (i.e. tipping points in ecosystems). This deficit stems largely from an inadequate understanding of the many complex interactions between species and the environment at the ecosystem level, and the paucity of mechanistic models relating environment to population dynamics at the species level. In marine ecosystems, abundant, short‐lived and fast‐growing species such as anchovies or squids, consistently function as ‘keystone’ groups whose population dynamics affect entire ecosystems. Increasing exploitation coupled with climate change impacts has the potential to affect these ecological groups and consequently, the entire marine ecosystem. There are currently very few models that predict the impact of climate change on these keystone groups. Here we use a combination of individual‐based bioenergetics and stage‐structured population models to characterize the fundamental capacity of cephalopods to respond to climate change. We demonstrate the potential for, and mechanisms behind, two unfavourable climate‐change‐induced thresholds in future population dynamics. Although one threshold was the direct consequence of a decrease in incubation time caused by ocean warming, the other threshold was linked to survivorship, implying the possibility of management through a modification of fishing mortality. Additional substantive changes in phenology were also predicted, with a possible loss in population resilience. Our results demonstrate the feasibility of predicting complex nonlinear dynamics with a reasonably simplistic mechanistic model, and highlight the necessity of developing such approaches for other species if attempts to moderate the impact of climate change on natural resources are to be effective.     

On the genetic parameter determining the efficiency of purging: an estimate for Drosophila egg‐to‐pupae viability

The consequences of inbreeding on fitness can be crucial in evolutionary and conservation grounds and depend upon the efficiency of purging against deleterious recessive alleles. Recently, analytical expressions have been derived to predict the evolution of mean fitness, taking into account both inbreeding and purging, which depend on an ‘effective purging coefficient (d_e)’. Here, we explore the validity of that predictive approach and assay the strength of purging by estimating d_e for egg‐to‐pupae viability (EPV) after a drastic reduction in population size in a recently captured base population of Drosophila melanogaster. For this purpose, we first obtained estimates of the inbreeding depression rate (δ) for EPV in the base population, and we found that about 40% was due to segregating recessive lethals. Then, two sets of lines were founded from this base population and were maintained with different effective size throughout the rest of the experiment (N = 6; N = 12), their mean EPV being assayed at different generations. Due to purging, the reductions in mean EPV experienced by these lines were considerably smaller than the corresponding neutral predictions. For the 60% of δ attributable to nonlethal deleterious alleles, our results suggest an effective purging coefficient d_e > 0.02. Similarly, we obtain that d_e > 0.09 is required to roughly account for purging against the pooled inbreeding depression from lethal and nonlethal deleterious alleles. This implies that purging should be efficient for population sizes of the order of a few tens and larger, but might be inefficient against nonlethal deleterious alleles in smaller populations.     

High‐throughput SNPs for all: genotyping‐in‐thousands

Understanding the genetic structure of species is essential for conservation. It is only with this information that managers, academics, user groups and land‐use planners can understand the spatial scale of migration and local adaptation, source‐sink dynamics and effective population size. Such information is essential for a multitude of applications including delineating management units, balancing management priorities, discovering cryptic species and implementing captive breeding programmes. Species can range from locally adapted by hundreds of metres (Pavey et al. 2010 ) to complete species panmixia (Côté et al. 2013 ). Even more remarkable is that this essential information can be obtained without fully sequenced or annotated genomes, but from mere (putatively) nonfunctional variants. First with allozymes, then microsatellites and now SNPs, this neutral genetic variation carries a wealth of information about migration and drift. For many of us, it may be somewhat difficult to remember our understanding of species conservation before the widespread usage of these useful tools. However most species on earth have yet to give us that ‘peek under the curtain’. With the current diversity on earth estimated to be nearly 9 million species (Mora et al. 2011 ), we have a long way to go for a comprehensive meta‐phylogeographic understanding. A method presented in this issue by Campbell and colleagues (Campbell et al. 2015 ) is a tool that will accelerate the pace in this area. Genotyping‐in‐thousands (GT‐seq) leverages recent advancements in sequencing technology to save many hours and dollars over previous methods to generate this important neutral genetic information.     

A resource of genome‐wide single‐nucleotide polymorphisms generated by RAD tag sequencing in the critically endangered European eel

Reduced representation genome sequencing such as restriction‐site‐associated DNA (RAD) sequencing is finding increased use to identify and genotype large numbers of single‐nucleotide polymorphisms (SNPs) in model and nonmodel species. We generated a unique resource of novel SNP markers for the European eel using the RAD sequencing approach that was simultaneously identified and scored in a genome‐wide scan of 30 individuals. Whereas genomic resources are increasingly becoming available for this species, including the recent release of a draft genome, no genome‐wide set of SNP markers was available until now. The generated SNPs were widely distributed across the eel genome, aligning to 4779 different contigs and 19 703 different scaffolds. Significant variation was identified, with an average nucleotide diversity of 0.00529 across individuals. Results varied widely across the genome, ranging from 0.00048 to 0.00737 per locus. Based on the average nucleotide diversity across all loci, long‐term effective population size was estimated to range between 132 000 and 1 320 000, which is much higher than previous estimates based on microsatellite loci. The generated SNP resource consisting of 82 425 loci and 376 918 associated SNPs provides a valuable tool for future population genetics and genomics studies and allows for targeting specific genes and particularly interesting regions of the eel genome.     

Density‐dependent effects on reproductive performance in a recovering population of White‐tailed Eagles Haliaeetus albicilla

Understanding the mechanisms that shape density‐dependent processes and population dynamics is often essential for species conservation. Two key mechanisms of density‐dependent reductions in reproductive performance are a limited access to foraging habitats (the habitat heterogeneity hypothesis) and territorial aggression towards conspecifics (the interference competition hypothesis) at high population densities. Disentangling the relative importance of these mechanisms within populations below their carrying capacity is important for the evaluation of the success of conservation measures. However, relatively few studies have attempted to quantify the relative importance of both mechanisms for the reproductive performance of a population. Many raptor populations are ideal model systems to investigate density‐dependent effects because they are currently recovering from human‐induced reductions during the last decades. Using a 14‐year dataset, we combined analyses of individual reproductive performance with a mechanistic population model to investigate early signs of density‐dependent regulation in a population of White‐tailed Eagles Haliaeetus albicilla in north‐east Germany. We found a negative effect of the number of neighbouring breeding pairs and a positive effect of water surface area (as a proxy for the availability of favourable foraging habitat) on breeding success and on the average number of nestlings. The mean nearest neighbour distance between breeding pairs has decreased, and the mean distance of nests to the nearest water body has increased over the last 14 years. Moreover, the population model indicates that even though the population is still growing, carrying capacity could be reached at about 500–950 territorial pairs. These results suggest that the selection of nesting sites is determined by a trade‐off between the distance to favourable foraging habitat and the distance to neighbouring breeding pairs. To avoid increasing competition with conspecifics, due to continued population growth, breeding pairs seem to select increasingly suboptimal habitats. Therefore, our results suggest that the habitat heterogeneity and interference competition hypotheses are not necessarily mutually exclusive as mechanisms of density‐dependent population regulation, but can determine the reproductive performance of a raptor population simultaneously. Thus, a future decline in breeding success does not necessarily reflect a decrease in habitat quality but may rather be a consequence of density‐dependent mechanisms. This information may be useful for the interpretation of population trends and for the development of appropriate management strategies for recovering raptor populations.     

Seasonal temperature and precipitation regulate brook trout young‐of‐the‐year abundance and population dynamics

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A population‐averaged approach to diagnostic test meta‐analysis

The meta‐analysis of diagnostic accuracy studies is often of interest in screening programs for many diseases. The typical summary statistics for studies chosen for a diagnostic accuracy meta‐analysis are often two dimensional: sensitivities and specificities. The common statistical analysis approach for the meta‐analysis of diagnostic studies is based on the bivariate generalized linear‐mixed model (BGLMM), which has study‐specific interpretations. In this article, we present a population‐averaged (PA) model using generalized estimating equations (GEE) for making inference on mean specificity and sensitivity of a diagnostic test in the population represented by the meta‐analytic studies. We also derive the marginalized counterparts of the regression parameters from the BGLMM. We illustrate the proposed PA approach through two dataset examples and compare performance of estimators of the marginal regression parameters from the PA model with those of the marginalized regression parameters from the BGLMM through Monte Carlo simulation studies. Overall, both marginalized BGLMM and GEE with sandwich standard errors maintained nominal 95% confidence interval coverage levels for mean specificity and mean sensitivity in meta‐analysis of 25 of more studies even under misspecification of the covariance structure of the bivariate positive test counts for diseased and nondiseased subjects.     

Development and testing of a genetic marker‐based pedigree reconstruction system ‘PR‐genie’ incorporating size‐class data

For wildlife populations, it is often difficult to determine biological parameters that indicate breeding patterns and population mixing, but knowledge of these parameters is essential for effective management. A pedigree encodes the relationship between individuals and can provide insight into the dynamics of a population over its recent history. Here, we present a method for the reconstruction of pedigrees for wild populations of animals that live long enough to breed multiple times over their lifetime and that have complex or unknown generational structures. Reconstruction was based on microsatellite genotype data along with ancillary biological information: sex and observed body size class as an indicator of relative age of individuals within the population. Using body size‐class data to infer relative age has not been considered previously in wildlife genealogy and provides a marked improvement in accuracy of pedigree reconstruction. Body size‐class data are particularly useful for wild populations because it is much easier to collect noninvasively than absolute age data. This new pedigree reconstruction system, PR‐genie, performs reconstruction using maximum likelihood with optimization driven by the cross‐entropy method. We demonstrated pedigree reconstruction performance on simulated populations (comparing reconstructed pedigrees to known true pedigrees) over a wide range of population parameters and under assortative and intergenerational mating schema. Reconstruction accuracy increased with the presence of size‐class data and as the amount and quality of genetic data increased. We provide recommendations as to the amount and quality of data necessary to provide insight into detailed familial relationships in a wildlife population using this pedigree reconstruction technique.     

In defence of model‐based inference in phylogeography

Recent papers have promoted the view that model‐based methods in general, and those based on Approximate Bayesian Computation (ABC) in particular, are flawed in a number of ways, and are therefore inappropriate for the analysis of phylogeographic data. These papers further argue that Nested Clade Phylogeographic Analysis (NCPA) offers the best approach in statistical phylogeography. In order to remove the confusion and misconceptions introduced by these papers, we justify and explain the reasoning behind model‐based inference. We argue that ABC is a statistically valid approach, alongside other computational statistical techniques that have been successfully used to infer parameters and compare models in population genetics. We also examine the NCPA method and highlight numerous deficiencies, either when used with single or multiple loci. We further show that the ages of clades are carelessly used to infer ages of demographic events, that these ages are estimated under a simple model of panmixia and population stationarity but are then used under different and unspecified models to test hypotheses, a usage the invalidates these testing procedures. We conclude by encouraging researchers to study and use model‐based inference in population genetics.     

Imputation of missing genotypes from low‐ to high‐density SNP panel in different population designs

Imputation of missing genotypes, in particular from low density to high density, is an important issue in genomic selection and genome‐wide association studies. Given the marker densities, the most important factors affecting imputation accuracy are the size of the reference population and the relationship between individuals in the reference (genotyped with high‐density panel) and study (genotyped with low‐density panel) populations. In this study, we investigated the imputation accuracies when the reference population (genotyped with Illumina BovineSNP50 SNP panel) contained sires, halfsibs, or both sires and halfsibs of the individuals in the study population (genotyped with Illumina BovineLD SNP panel) using three imputation programs (fimpute v2.2, findhap v2, and beagle v3.3.2). Two criteria, correlation between true and imputed genotypes and missing rate after imputation, were used to evaluate the performance of the three programs in different scenarios. Our results showed that fimpute performed the best in all cases, with correlations from 0.921 to 0.978 when imputing from sires to their daughters or between halfsibs. In general, the accuracies of imputing between halfsibs or from sires to their daughters were higher than were those imputing between non‐halfsibs or from sires to non‐daughters. Including both sires and halfsibs in the reference population did not improve the imputation performance in comparison with when only including halfsibs in the reference population for all the three programs.     

A genetic demographic analysis of Lake Malawi rock‐dwelling cichlids using spatio‐temporal sampling

We estimated the effective population sizes (N_e) and tested for short‐term temporal demographic stability of populations of two Lake Malawi cichlids: Maylandia benetos, a micro‐endemic, and Maylandia zebra, a widespread species found across the lake. We sampled a total of 351 individuals, genotyped them at 13 microsatellite loci and sequenced their mitochondrial D‐loop to estimate genetic diversity, population structure, demographic history and effective population sizes. At the microsatellite loci, genetic diversity was high in all populations. Yet, genetic diversity was relatively low for the sequence data. Microsatellites yielded mean N_e estimates of 481 individuals (±99 SD) for M. benetos and between 597 (±106.3 SD) and 1524 (±483.9 SD) individuals for local populations of M. zebra. The microsatellite data indicated no deviations from mutation–drift equilibrium. Maylandia zebra was further found to be in migration–drift equilibrium. Temporal fluctuations in allele frequencies were limited across the sampling period for both species. Bayesian Skyline analyses suggested a recent expansion of M. zebra populations in line with lake‐level fluctuations, whereas the demographic history of M. benetos could only be estimated for the very recent past. Divergence time estimates placed the origin of M. benetos within the last 100 ka after the refilling of the lake and suggested that it split off the sympatric M. zebra population. Overall, our data indicate that micro‐endemics and populations in less favourable habitats have smaller N_e, indicating that drift may play an important role driving their divergence. Yet, despite small population sizes, high genetic variation can be maintained.     

Linked‐read sequencing enables haplotype‐resolved resequencing at population scale

The feasibility to sequence entire genomes of virtually any organism provides unprecedented insights into the evolutionary history of populations and species. Nevertheless, many population genomic inferences – including the quantification and dating of admixture, introgression and demographic events, and inference of selective sweeps – are still limited by the lack of high‐quality haplotype information. The newest generation of sequencing technology now promises significant progress. To establish the feasibility of haplotype‐resolved genome resequencing at population scale, we investigated properties of linked‐read sequencing data of songbirds of the genus Oenanthe across a range of sequencing depths. Our results based on the comparison of downsampled (25×, 20×, 15×, 10×, 7×, and 5×) with high‐coverage data (46–68×) of seven bird genomes mapped to a reference suggest that phasing contiguities and accuracies adequate for most population genomic analyses can be reached already with moderate sequencing effort. At 15× coverage, phased haplotypes span about 90% of the genome assembly, with 50% and 90% of phased sequences located in phase blocks longer than 1.25–4.6 Mb (N50) and 0.27–0.72 Mb (N90). Phasing accuracy reaches beyond 99% starting from 15× coverage. Higher coverages yielded higher contiguities (up to about 7 Mb/1 Mb [N50/N90] at 25× coverage), but only marginally improved phasing accuracy. Phase block contiguity improved with input DNA molecule length; thus, higher‐quality DNA may help keeping sequencing costs at bay. In conclusion, even for organisms with gigabase‐sized genomes like birds, linked‐read sequencing at moderate depth opens an affordable avenue towards haplotype‐resolved genome resequencing at population scale.     

Determinants of species‐area relationships for marsh‐nesting birds

ABSTRACT To clarify the underlying causes of the species‐area relationship in marsh‐nesting birds, I studied eight freshwater tidal marshes of the Connecticut River that differed in area, degree of isolation, mudflat cover, water cover, tidal regime, and extent of individual plant communities. I measured these habitat variables on aerial infrared photos, and surveyed bird populations by mapping the distribution of all birds in marshes under 5 ha in area and establishing 50‐m radius plots in marshes over 5 ha. From surveys, I determined species richness, population densities, and total populations. Analysis revealed a positive relationship between species richness and area, but no correlation between area and habitat heterogeneity. Other habitat variables were poor predictors of species richness. The lack of a relationship between habitat and species richness appeared to be a consequence of most vegetation types present not being sufficiently distinct for birds to differentially associate with them. I also found no relationship between bird population density and area, suggesting that habitat quality in marshes did not improve with increasing size, and species evenness declined with increasing richness because greater richness was associated with the presence of more rare species. Larger marshes had more rare species, species with larger populations, and species with a minimum threshold area for occurrence. Thus, my results are consistent with theoretical predictions that larger populations are less prone to local extinction and, as individuals are added to a community, more rare species are present.     

Likelihood‐based inference of population history from low‐coverage de novo genome assemblies

Short‐read sequencing technologies have in principle made it feasible to draw detailed inferences about the recent history of any organism. In practice, however, this remains challenging due to the difficulty of genome assembly in most organisms and the lack of statistical methods powerful enough to discriminate between recent, nonequilibrium histories. We address both the assembly and inference challenges. We develop a bioinformatic pipeline for generating outgroup‐rooted alignments of orthologous sequence blocks from de novo low‐coverage short‐read data for a small number of genomes, and show how such sequence blocks can be used to fit explicit models of population divergence and admixture in a likelihood framework. To illustrate our approach, we reconstruct the Pleistocene history of an oak‐feeding insect (the oak gallwasp Biorhiza pallida), which, in common with many other taxa, was restricted during Pleistocene ice ages to a longitudinal series of southern refugia spanning the Western Palaearctic. Our analysis of sequence blocks sampled from a single genome from each of three major glacial refugia reveals support for an unexpected history dominated by recent admixture. Despite the fact that 80% of the genome is affected by admixture during the last glacial cycle, we are able to infer the deeper divergence history of these populations. These inferences are robust to variation in block length, mutation model and the sampling location of individual genomes within refugia. This combination of de novo assembly and numerical likelihood calculation provides a powerful framework for estimating recent population history that can be applied to any organism without the need for prior genetic resources.     

Long‐term mark‐and‐recapture study of a freshwater mussel reveals patterns of habitat use and an association between survival and river discharge

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Census data aggregation decisions can affect population‐level inference in heterogeneous populations

1. Conservation and population management decisions often rely on population models parameterized using census data. However, the sampling regime, precision, sample size, and methods used to collect census data are usually heterogeneous in time and space. Decisions about how to derive population‐wide estimates from this patchwork of data are complicated and may bias estimated population dynamics, with important implications for subsequent management decisions.
2. Here, we explore the impact of site selection and data aggregation decisions on pup survival estimates, and downstream estimates derived from parameterized matrix population models (MPMs), using a long‐term dataset on grey seal (Halichoerus grypus) pup survival from southwestern Wales. The spatiotemporal and methodological heterogeneity of the data are fairly typical for ecological census data and it is, therefore, a good model to address this topic.
3. Data were collected from 46 sampling locations (sites) over 25 years, and we explore the impact of data handling decisions by varying how years and sampling locations are combined to parameterize pup survival in population‐level MPMs. We focus on pup survival because abundant high‐quality data are available on this developmental stage.
4. We found that survival probability was highly variable with most variation being at the site level, and poorly correlated among sampling sites. This variation could generate marked differences in predicted population dynamics depending on sampling strategy. The sample size required for a confident survival estimate also varied markedly geographically.
5. We conclude that for populations with highly variable vital rates among sub‐populations, site selection and data aggregation methods are important. In particular, including peripheral or less frequently used areas can introduce substantial variation into population estimates. This is likely to be context‐dependent, but these choices, including the use of appropriate weights when summarizing across sampling areas, should be explored to ensure that management actions are successful.

     

Genetic diversity,population structure and sex‐biased dispersal in three co‐evolving species

Genetic diversity and spatial structure of populations are important for antagonistic coevolution. We investigated genetic variation and population structure of three closely related European ant species: the social parasite Harpagoxenus sublaevis and its two host species Leptothorax acervorum and Leptothorax muscorum. We sampled populations in 12 countries and analysed eight microsatellite loci and an mtDNA sequence. We found high levels of genetic variation in all three species, only slightly less variation in the host L. muscorum. Using a newly introduced measure of differentiation (Jost’s D_est ), we detected strong population structuring in all species and less male‐biased dispersal than previously thought. We found no phylogeographic patterns that could give information on post‐glacial colonization routes – northern populations are as variable as more southern populations. We conclude that conditions for Thompson’s geographic mosaic of coevolution are ideal in this system: all three species show ample genetic variation and strong population structure.     

Using time‐of‐detection to evaluate detectability assumptions in temporally replicated aural count indices: an example with Ring‐necked Pheasants

ABSTRACT The validity of treating counts as indices to abundance is based on the assumption that the expected detection probability, E(p), is constant over time or comparison groups or, more realistically, that variation in p is small relative to variation in population size that investigators seek to detect. Unfortunately, reliable estimates of E(p) and var(p) are lacking for most index methods. As a case study, we applied the time‐of‐detection method to temporally replicated (within season) aural counts of crowing male Ring‐necked Pheasants (Phasianus colchicus) at 18 sites in southern Minnesota in 2007 to evaluate the detectability assumptions. More specifically, we used the time‐of‐detection method to estimate E(p) and var(p), and then used these estimates in a Monte Carlo simulation to evaluate bias‐variance tradeoffs associated with adjusting count indices for imperfect detection. The estimated mean detection probability in our case study was 0.533 (SE = 0.030) and estimated spatial variation in E(p) was 0.081 (95% CI: 0.057–0.126). On average, both adjusted (for) and unadjusted counts of crowing males qualitatively described the simulated relationship between pheasant abundance and grassland abundance, but the bias‐variance tradeoff was smaller for adjusted counts (MSE = 0.003 vs. 0.045, respectively). Our case study supports the general recommendation to use, whenever feasible, formal population‐estimation procedures (e.g., mark‐recapture, distance sampling, double sampling) to account for imperfect detection. However, we caution that interpreting estimates of absolute abundance can be complicated, even if formal estimation methods are used. For example, the time‐of‐detection method was useful for evaluating detectability assumptions in our case study and the method could be used to adjust aural count indices for imperfect detection. Conversely, using the time‐of‐detection method to estimate absolute abundances in our case study was problematic because the biological populations and sampling coverage could not be clearly delineated. These estimation and inference challenges may also be important in other avian surveys that involve mobile species (whose home ranges may overlap several sampling sites), temporally replicated counts, and inexact sampling coverage.     

Male‐mimicking females increase male‐male interactions,and decrease male survival and condition in a female‐polymorphic damselfly

Biologists are still discovering diverse and powerful ways sexual conflicts shape biodiversity. The present study examines how the proportion of females in a population that exhibit male mimicry, a mating resistance trait, influences conspecific males’ behavior, condition, and survival. Like most female‐polymorphic damselflies, Ischnura ramburii harbors both “andromorph” females, which closely resemble males, and sexually dimorphic “gynomorph” counterparts. There is evidence that male mimicry helps andromorphs evade detection and harassment, but males can also learn to target locally prevalent morph(s) via prior mate encounters. I hypothesized that the presence of male mimics could therefore predispose males to mate recognition errors, and thereby increase rates of costly male‐male interactions. Consistent with this hypothesis, male‐male interaction rates were highest in mesocosms containing more andromorph (vs. gynomorph) females. Males in andromorph‐biased mesocosms also had lower final body mass and higher mortality than males assigned to gynomorph‐majority treatments. Male survival and body mass were each negatively affected by mesocosm density, and mortality data revealed a marginally significant interaction between andromorph frequency and population density. These findings suggest that, under sufficiently crowded conditions, female mating resistance traits such as male mimicry could have pronounced indirect effects on male behavior, condition, and survival.     

Genetic population structure in prickly sculpin (Cottus asper) reflects isolation‐by‐environment between two life‐history ecotypes

Life‐history transitions have evolved repeatedly in numerous taxa, although the ecological and evolutionary conditions favouring such transitions in the presence of gene flow remain poorly understood. The present study aimed to disentangle the effects of isolation‐by‐distance and isolation‐by‐environment on genetic differentiation between two sympatric life‐history ecotypes. Using 14 microsatellite loci, we first characterized amphidromous and freshwater groups of Cottus asper in a high gene flow setting in the Lower Fraser River system (south‐western British Columbia, Canada) to test for the effects of habitat and geographical distance on the distribution of life‐history ecotypes. Within the main river channel, no genetic differentiation was found, whereas tributaries even close to the estuary were genetically differentiated. Partial mantel tests confirmed that genetic differentiation between river tributaries and the main channel was independent from geographical distance, with distance‐scaled migration rates indicating reduced gene flow from the main channel into the tributaries. Our results suggest that isolation‐by‐environment can play an important role for the early stage of life‐history transitions, and may promote differentiation among life‐history ecotypes despite the presence of gene flow. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 943–957.