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Concept: Effective population size

132

The ongoing refugee crisis in Europe has seen many countries rush to construct border security fencing to divert or control the flow of people. This follows a trend of border fence construction across Eurasia during the post-9/11 era. This development has gone largely unnoticed by conservation biologists during an era in which, ironically, transboundary cooperation has emerged as a conservation paradigm. These fences represent a major threat to wildlife because they can cause mortality, obstruct access to seasonally important resources, and reduce effective population size. We summarise the extent of the issue and propose concrete mitigation measures.

Concepts: Minimum viable population, Conservation biology, Population size, Europe, Effective population size, Fencing, Population genetics, Population ecology

40

The Kalash represent an enigmatic isolated population of Indo-European speakers who have been living for centuries in the Hindu Kush mountain ranges of present-day Pakistan. Previous Y chromosome and mitochondrial DNA markers provided no support for their claimed Greek descent following Alexander III of Macedon’s invasion of this region, and analysis of autosomal loci provided evidence of a strong genetic bottleneck. To understand their origins and demography further, we genotyped 23 unrelated Kalash samples on the Illumina HumanOmni2.5M-8 BeadChip and sequenced one male individual at high coverage on an Illumina HiSeq 2000. Comparison with published data from ancient hunter-gatherers and European farmers showed that the Kalash share genetic drift with the Paleolithic Siberian hunter-gatherers and might represent an extremely drifted ancient northern Eurasian population that also contributed to European and Near Eastern ancestry. Since the split from other South Asian populations, the Kalash have maintained a low long-term effective population size (2,319-2,603) and experienced no detectable gene flow from their geographic neighbors in Pakistan or from other extant Eurasian populations. The mean time of divergence between the Kalash and other populations currently residing in this region was estimated to be 11,800 (95% confidence interval = 10,600-12,600) years ago, and thus they represent present-day descendants of some of the earliest migrants into the Indian sub-continent from West Asia.

Concepts: Population ecology, South Asia, Population bottleneck, Effective population size, Afghanistan, Asia, Indian subcontinent, Population genetics

29

The 50/500 rule has been used as a guiding principle in conservation for assessing minimum viable effective population size (N(e)). There is much confusion in the recent literature about how the 500 value should be applied to assess extinction risk and set priorities in conservation biology. Here, we argue that the confusion arises when the genetic basis for a short-term N(e) of 50 to avoid inbreeding depression is used to justify a long-term N(e) of 500 to maintain evolutionary potential. This confusion can result in misleading conclusions about how genetic arguments alone are sufficient to set minimum viable population (MVP) thresholds for assessing the extinction risk of threatened species, especially those that emphasize that MVPs should be in the thousands to maintain evolutionary potential.

Concepts: Species, Extinction, Effective population size, Conservation biology, Minimum viable population, Population bottleneck, Evolution, Population genetics

11

The Scandinavian wolf population descends from only five individuals, is isolated, highly inbred and exhibits inbreeding depression. To meet international conservation goals, suggestions include managing subdivided wolf populations over Fennoscandia as a metapopulation; a genetically effective population size of Ne⩾500, in line with the widely accepted long-term genetic viability target, might be attainable with gene flow among subpopulations of Scandinavia, Finland and Russian parts of Fennoscandia. Analytical means for modeling Ne of subdivided populations under such non-idealized situations have been missing, but we recently developed new mathematical methods for exploring inbreeding dynamics and effective population size of complex metapopulations. We apply this theory to the Fennoscandian wolves using empirical estimates of demographic parameters. We suggest that the long-term conservation genetic target for metapopulations should imply that inbreeding rates in the total system and in the separate subpopulations should not exceed Δf=0.001. This implies a meta-Ne of NeMeta⩾500 and a realized effective size of each subpopulation of NeRx⩾500. With current local effective population sizes and one migrant per generation, as recommended by management guidelines, the meta-Ne that can be reached is ~250. Unidirectional gene flow from Finland to Scandinavia reduces meta-Ne to ~130. Our results indicate that both local subpopulation effective sizes and migration among subpopulations must increase substantially from current levels to meet the conservation target. Alternatively, immigration from a large (Ne⩾500) population in northwestern Russia could support the Fennoscandian metapopulation, but immigration must be substantial (5-10 effective immigrants per generation) and migration among Fennoscandian subpopulations must nevertheless increase.Heredity advance online publication, 22 June 2016; doi:10.1038/hdy.2016.44.

Concepts: Scandinavian Peninsula, Population, Finland, Demography, Immigration, Effective population size, Population ecology, Population genetics

7

The current conservation status of the bottlenose dolphin (Tursiops truncatus) under the IUCN is ‘least concern’. However, in the Caribbean, small and localized populations of the ‘inshore form’ may be at higher risk of extinction than the ‘worldwide distributed form’ due to a combination of factors including small population size, high site fidelity, genetic isolation, and range overlap with human activities. Here, we study the population genetic structure of bottlenose dolphins from the Archipelago of Bocas del Toro in Panama. This is a small population characterized by high site fidelity and is currently heavily-impacted by the local dolphin-watching industry. We collected skin tissue samples from 25 dolphins to study the genetic diversity and structure of this population. We amplified a portion of the mitochondrial Control Region (mtDNA-CR) and nine microsatellite loci. The mtDNA-CR analyses revealed that dolphins in Bocas del Toro belong to the ‘inshore form’, grouped with the Bahamas-Colombia-Cuba-Mexico population unit. They also possess a unique haplotype new for the Caribbean. The microsatellite data indicated that the Bocas del Toro dolphin population is highly structured, likely due to restricted movement patterns. Previous abundance estimates obtained with mark-recapture methods reported a small population of 80 dolphins (95% CI = 72-87), which is similar to the contemporary effective population size estimated in this study (Ne = 73 individuals; CI = 18.0 - ∞; 0.05). The combination of small population size, high degree of genetic isolation, and intense daily interactions with dolphin-watching boats puts the Bocas del Toro dolphin to at high risk of extinction. Despite national guidelines to regulate the dolphin-watching industry in Bocas del Toro and ongoing educational programs for tour operators, only in 2012 seven animals have died due to boat collisions. Our results suggest that the conservation status of bottlenose dolphins in Bocas del Toro should be elevated to ‘endangered’ at the national level, as a precautionary measure while population and viability estimates are conducted.

Concepts: Population ecology, Effective population size, Common Bottlenose Dolphin, Great white shark, Animal echolocation, Bottlenose dolphin, Cetacean intelligence, Population genetics

6

By combining high-throughput sequencing (HTS) with experimental evolution, we can observe the within-host dynamics of pathogen variants of biomedical or ecological interest. We studied the evolutionary dynamics of five variants of Potato virus Y (PVY) in 15 doubled-haploid lines of pepper. All plants were inoculated with the same mixture of virus variants and, variant frequencies were determined by HTS in eight plants of each pepper line, at each of six sampling dates. We developed a method for estimating the intensities of selection and genetic drift in a multi-allelic Wright-Fisher model, applicable whether these forces are strong or weak, and in the absence of neutral markers. This method requires variant frequency determination at several time points, in independent hosts. The parameters are the selection coefficients for each PVY variant and four effective population sizes Ne at different time-points of the experiment. Numerical simulations of asexual haploid Wright-Fisher populations subjected to contrasting genetic drift (Ne ∈ [10, 2000]) and selection (|s| ∈ [0, 0.15]) regimes were used to validate the method proposed. The experiment in closely related pepper host genotypes revealed that viruses experienced a considerable diversity of selection and genetic drift regimes. The resulting variant dynamics were accurately described by Wright-Fisher models. The fitness ranks of the variants were almost identical between host genotypes. By contrast, the dynamics of Ne were highly variable, although a bottleneck was often identified during the systemic movement of the virus. We demonstrated that, for a fixed initial PVY population, virus effective population size is a heritable trait in plants. These findings pave the way for the breeding of plant varieties exposing viruses to stronger genetic drift, thereby slowing virus adaptation.

Concepts: Potato virus Y, Population ecology, Genetic drift, Population bottleneck, Effective population size, Evolution, Genetics, Population genetics

4

Semi-natural grassland areas expanded worldwide several thousand years ago following an increase in anthropogenic activities. However, semi-natural grassland habitat areas have been declining in recent decades due to changes in landuse, which have caused a loss of grassland biodiversity. Reconstructing historical and recent demographic changes in semi-natural grassland species will help clarify the factors affecting their population decline. Here we quantified past and recent demographic histories of Melitaea ambigua (Lepidoptera; Nymphalidae), an endangered grassland butterfly species in Japan. We examined changes in demography over the past 10,000 years based on 1378 bp of mitochondrial COI gene. We then examined changes in its genetic diversity and structure during the last 30 years using nine microsatellite DNA markers. The effective population size of M. ambigua increased about 3000-6000 years ago. In contrast, the genetic diversity and effective population sizes of many populations significantly declined from the 1980s to 2010s, which is consistent with a recent decline in the species population size. Our data suggest that the M. ambigua demography can be traced to changes in area covered by semi-natural grasslands throughout the Holocene.

Concepts: Demographic economics, Biodiversity, Population size, Effective population size, Population ecology, Butterfly, Demography, Population genetics

4

Island endemics are expected to have low effective population sizes (Ne), firstly because some may experience population bottlenecks when they are founded, and secondly because they have restricted ranges. Therefore we expect island species to have reduced genetic diversity, inefficient selection and reduced adaptive potential compared to their mainland counterparts. We used both polymorphism and substitution data to address these predictions, improving on the approach of recent studies that only used substitution data. This allowed us to directly test the assumption that island species have small values of Ne We found that island species had significantly less genetic diversity than mainland species; however, this pattern could be attributed to a subset of island species that appeared to have undergone a recent population bottleneck. When these species were excluded from the analysis, island and mainland species had similar levels of genetic diversity, despite island species occupying considerably smaller areas than their mainland counterparts. We also found no overall difference between island and mainland species in terms of the effectiveness of selection or the mutation rate. Our evidence suggests that island colonisation has no lasting impact on molecular evolution. This surprising result highlights gaps in our knowledge of the relationship between census and effective population size.

Concepts: DNA, Population ecology, Population size, Genetic drift, Effective population size, Population bottleneck, Evolution, Population genetics

4

Bees are the primary pollinators of flowering plants in almost all ecosystems. Worldwide declines in bee populations have raised awareness about the importance of their ecological role in maintaining ecosystem functioning. The naturally strong philopatric behavior that some bee species show can be detrimental to population viability through increased probability of inbreeding. Furthermore, bee populations found in human-altered landscapes, such as urban areas, can experience lower levels of gene flow and effective population sizes, increasing potential for inbreeding depression in wild bee populations. In this study, we investigated the fine-scale population structure of the solitary bee Colletes inaequalis in an urbanized landscape. First, we developed a predictive spatial model to detect suitable nesting habitat for this ground nesting bee and to inform our field search for nests. We genotyped 18 microsatellites in 548 female individuals collected from nest aggregations throughout the study area. Genetic relatedness estimates revealed that genetic similarity among individuals was slightly greater within nest aggregations than among randomly chosen individuals. However, genetic structure among nest aggregations was low (Nei’s GST = 0.011). Reconstruction of parental genotypes revealed greater genetic relatedness among females than among males within nest aggregations, suggesting male-mediated dispersal as a potentially important mechanism of population connectivity and inbreeding avoidance. Size of nesting patch was positively correlated with effective population size, but not with other estimators of genetic diversity. We detected a positive trend between geographic distance and genetic differentiation between nest aggregations. Our landscape genetic models suggest that increased urbanization is likely associated with higher levels of inbreeding. Overall, these findings emphasize the importance of density and distribution of suitable nesting patches for enhancing bee population abundance and connectivity in human dominated habitats and highlights the critical contribution of landscape genetic studies for enhanced conservation and management of native pollinators.

Concepts: Minimum viable population, Population size, Effective population size, Genetics, Ecology, Population ecology, Bee, Population genetics

4

Profound knowledge of demographic history is a prerequisite for the understanding and inference of processes involved in the evolution of population differentiation and speciation. Together with new coalescent-based methods, the recent availability of genome-wide data enables investigation of differentiation and divergence processes at unprecedented depth. We combined two powerful approaches, full Approximate Bayesian Computation analysis (ABC) and pairwise sequentially Markovian coalescent modeling (PSMC), to reconstruct the demographic history of the split between two avian speciation model species, the pied flycatcher and collared flycatcher. Using whole-genome re-sequencing data from 20 individuals, we investigated 15 demographic models including different levels and patterns of gene flow, and changes in effective population size over time. ABC provided high support for recent (mode 0.3 my, range <0.7 my) species divergence, declines in effective population size of both species since their initial divergence, and unidirectional recent gene flow from pied flycatcher into collared flycatcher. The estimated divergence time and population size changes, supported by PSMC results, suggest that the ancestral species persisted through one of the glacial periods of middle Pleistocene and then split into two large populations that first increased in size before going through severe bottlenecks and expanding into their current ranges. Secondary contact appears to have been established after the last glacial maximum. The severity of the bottlenecks at the last glacial maximum is indicated by the discrepancy between current effective population sizes (20,000-80,000) and census sizes (5-50 million birds) of the two species. The recent divergence time challenges the supposition that avian speciation is a relatively slow process with extended times for intrinsic postzygotic reproductive barriers to evolve. Our study emphasizes the importance of using genome-wide data to unravel tangled demographic histories. Moreover, it constitutes one of the first examples of the inference of divergence history from genome-wide data in non-model species.

Concepts: Population ecology, Population size, Glacial period, Effective population size, Last glacial period, Last Glacial Maximum, Ice age, Pleistocene