Yvonne Verkuil | University of Groningen (original) (raw)

Papers by Yvonne Verkuil

Biological Conservation, 2012

Nature genetics, Jan 16, 2015

Three strikingly different alternative male mating morphs (aggressive 'independents', sem... more Three strikingly different alternative male mating morphs (aggressive 'independents', semicooperative 'satellites' and female-mimic 'faeders') coexist as a balanced polymorphism in the ruff, Philomachus pugnax, a lek-breeding wading bird. Major differences in body size, ornamentation, and aggressive and mating behaviors are inherited as an autosomal polymorphism. We show that development into satellites and faeders is determined by a supergene consisting of divergent alternative, dominant and non-recombining haplotypes of an inversion on chromosome 11, which contains 125 predicted genes. Independents are homozygous for the ancestral sequence. One breakpoint of the inversion disrupts the essential CENP-N gene (encoding centromere protein N), and pedigree analysis confirms the lethality of homozygosity for the inversion. We describe new differences in behavior, testis size and steroid metabolism among morphs and identify polymorphic genes within the inversion t...

The Greenlandic and west-central Siberian breeding populations of Sanderlings Calidris alba are s... more The Greenlandic and west-central Siberian breeding populations of Sanderlings Calidris alba are separated by ca. 2000 km during the breeding season, but mix in Europe to some extent during migration. However, the number of Siberian Sanderlings that spend the nonbreeding season along the East Atlantic Flyway (extending from western Europe to South Africa), if any, is unknown. Although both populations are considered part of the nominate subspecies C. a. alba based on morphology, population structure in Sanderlings has yet to be described with molecular methods. We examined genetic differentiation at the mtDNA control region (CR) and seven microsatellite loci between Greenland- and Siberia-breeding Sanderlings in order to: (1) develop a diagnostic tool
for assessing the breeding origin of Sanderlings along the East Atlantic Flyway, and (2) provide a comparison with the co-distributed and ecologically similar Red Knot, in which CR differentiation of geographically analogous populations (C. canutus islandica and C. c. canutus) has indicated isolation of lineages near the time of the last glacial maximum. By contrast, we found only weak differentiation between the Sanderling breeding populations at the CR, and no differentiation at microsatellite loci. These results suggest that the assignment of breeding origin of Sanderlings on Afro-European flyways will not be possible with simple and inexpensive genetic methods, and imply that Sanderlings and Red Knots have very different
post-glacial phylogeographic histories.

The fuelling performance of long-distance migrants at staging areas indicates local conditions an... more The fuelling performance of long-distance migrants at staging areas indicates local conditions and determines the viability of migration routes. Here we present a first case study where long-term fuelling performance was documented along two migration routes with differential population trends. Ruffs (Philomachus pugnax) are shorebirds of inland freshwater wetlands that migrate from the sub-Saharan wintering grounds, via Europe, to the northern Eurasian breeding grounds. Assessments from 2001 to 2008 of fuelling during northward migration at the major western and eastern staging site revealed that daily mass gain rates steeply declined across years in the grasslands for dairy production in Friesland, The Netherlands, and remained constant in the Pripyat floodplains in Belarus, 1500 km further east. Migrants in Friesland decreased from 2001 to 2010 by 66%, amounting to a loss of 21,000 individuals when counts were adjusted for length of stay as determined by resightings. In the same period numbers in Pripyat increased by 12,000. Ruffs individually ringed in Friesland were resighted in subsequent springs at increasingly eastern sites including Pripyat. Our results corroborate published evidence for an eastward redistribution of Arctic breeding ruffs and suggest that the decreasing fuelling rates in the westernmost staging area contribute to this redistribution. The shift implies that responses occur within a single generation. The hypothesis that the choice of route during northward migration may be driven by food availability can now be tested by creating greater areas of wet grasslands in Friesland. When local staging conditions improve we predict that ruffs will make the reverse shift.

Diversity and …, Jan 1, 2010

Aim: Over the last two decades, thousands of northward migrating ruffs (Philomachus pugnax) have ... more Aim: Over the last two decades, thousands of northward migrating ruffs (Philomachus pugnax) have disappeared from western European staging sites. These migratory ruffs were partly temperate breeding birds, but most individuals head towards the Eurasian Arctic tundras where 95% of the global population breeds. This regional decline may represent either: (1) local loss of breeding birds in western Europe, (2) a global decline, (3) shift(s) in distribution or (4) a combination of these.

Location: Northern Eurasia.

Methods: To put the declines in western Europe in context, we analysed Arctic monitoring data from the last two decades (Soloviev & Tomkovich, 2009) to detect changes in regional breeding densities across northern Eurasia. We used a novel approach applying generalized additive modelling (GAM) and generalized estimations equations (GEE).

Results: We show that the global breeding population of ruffs has made a significant eastwards shift into the Asian part of the breeding range. In the European Arctic, ruffs decreased during the last 18 years. At the same time, in western Siberia, ruffs increased. In eastern Siberia, no significant population changes could be detected. These changes corroborate the finding that during northward migration, growing numbers of ruffs avoided staging areas in the Netherlands and Sweden and started migrating along a more easterly route leading into western Siberia.

Main conclusions: We detected an unprecedented large-scale population redistribution of ruffs and suggest that this is a response to loss of habitat quality at the traditional staging site in the Netherlands.

Long-distance migrant waders breeding in the Arctic often have globally structured populations, l... more Long-distance migrant waders breeding in the Arctic often have globally structured populations, largely because they were isolated in glacial or interstadial refugia or are restricted to fragmented coastal wetlands in winter. Conversely, inland species using continentally distributed wetlands appear to be less structured (more panmictic), presumably because they are less likely to have been isolated by multiple refugia or by current events. We analyzed genetic variation in a widely distributed inland species, the ruff (Philomachus pugnax), sampled from seven Eurasian breeding localities, and from migration routes and wintering areas in Europe and Africa. One mitochondrial marker (n = 118) and eight nuclear microsatellites (n = 170) showed (a) high genetic variation, (b) large genetic distances among mitochondrial (private) haplotypes within breeding populations, (c) the absence of a signature of isolation-by-distance, and (d) a distribution of private microsatellite alleles indicating dispersal between Scandinavia and Siberia, but not between western and East Siberia. These results were consistent with a large refugial population during the Last Glacial Maximum, and postglacial long range expansions spreading ancestral polymorphisms, and not with a stepping-stone model of gene flow. The divergence between breeding populations in Europe and Siberia was dated to about 12,000 years ago. Though genetic population structure is presently statistically nonexistent, support for evolving population structure came from analyses of geographic variation in two relevant phenotypic traits, wing length and timing of migration. Analysis of 6,077 individuals sampled on migration in 2002-08 revealed that in each year shorter-winged birds migrated through significantly later than longer-winged birds. The late-passing birds were associated with more westerly breeding localities. In conclusion, the lack of genetic structuring in ruffs (and other inland species we examined) contrasts with strong structuring in many coastal species which is in accordance with the hypothesis. This suggests that the ability to use more widely available inland habitat influences the evolution of genetic structure and the maintenance of genetic variation in waders.

Ecology and Evolution, 2014

Sex differences in skews of vertebrate lifetime reproductive success are difficult to measure dir... more Sex differences in skews of vertebrate lifetime reproductive success are difficult to measure directly. Evolutionary histories of differential skew should be detectable in the genome. For example, male-biased skew should reduce variation in the biparentally inherited genome relative to the maternally inherited genome. We tested this approach in lek-breeding ruff (Class Aves, Philomachus pugnax) by comparing genetic variation of nuclear microsatellites (theta-n; biparental) versus mitochondrial D-loop sequences (theta-m; maternal), and conversion to comparable nuclear (Ne) and female (Nef) effective population size using published ranges of mutation rates for each marker (l). We provide a Bayesian method to calculate Ne (theta-n = 4Ne*mu) and Nef (theta-m = 2Ne*mu) using 95% credible intervals (CI) of theta-n and theta-m as informative priors, and accounting for uncertainty in l. In 96 male ruffs from one population, Ne was 97% (79–100%) lower than expected under random mating in an ideal population, where Ne:Nef = 2. This substantially lower autosomal variation represents the first genomic support of strong male reproductive skew in a lekking species.

Conservation Genetics

With 40% of the European Black-tailed Godwit population breeding in The Netherlands, this country... more With 40% of the European Black-tailed Godwit population breeding in The Netherlands, this country harbours nternationally significant numbers of this species.However, ongoing agricultural intensification has resulted in the fragmentation of the population and drastic population declines since 1967. By establishing genetic diversity, genetic differentiation and gene flow on the basis of 12 microsatellites, we investigated whether the oopulation genetic structure of the Dutch Black-tailed Godwit bears the marks of these changes. Genetic diversity appeared to be moderate, and Bayesian model-based analysis of individual genotypes revealed no clustering in the Dutch populations. This was supported by pairwise FST values and AMOVA, which indicated no differentiation among the nine breeding areas. Gene flow estimates were larger than ‘‘one migrant per generation’’ between sample locations, and no isolation by distance was demonstrated. Our results indicate the maintenance of moderate levels of genetic diversity and genetic connectivity between breeding sites throughout the Dutch Black-tailed Godwit breeding population. We suggest that the Dutch Black-tailed Godwit breeding areas should be managed as a single panmictic unit, much as it is presently done.

Executive Summary The IUCN Species Survival Commission and IUCN Asia Regional Office commissioned... more Executive Summary The IUCN Species Survival Commission and IUCN Asia Regional Office commissioned this independent report to assess the state and condition of intertidal habitats along the East Asian-Australasian Flyway (EAAF), in response to growing concerns expressed by IUCN members over observed declines in biodiversity, the loss of ecological services, and an increase in ecological disasters.

Immunogenetics, 2013

The major histocompatibility complex (MHC) includes highly polymorphic gene families encoding pro... more The major histocompatibility complex (MHC) includes highly polymorphic gene families encoding proteins crucial to the vertebrate acquired immune system. Classical MHC class I (MHCI) genes code for molecules expressed on the surfaces of most nucleated cells and are associated with defense against intracellular pathogens, such as viruses. These genes have been studied in a few wild bird species, but have not been studied in long-distance migrating shorebirds. Red Knots Calidris canutus are medium-sized, monogamous sandpipers with migratory routes that span the globe. Understanding how such long-distance migrants protect themselves from disease has gained new relevance since the emergence of avian-borne diseases, including intracellular pathogens recognized by MHCI molecules, such as avian influenza. In this study, we characterized MHCI genes in knots and found 36 alleles in eight individuals and evidence for six putatively functional and expressed MHCI genes in a single bird. We also found evidence for recombination and for positive selection at putative peptide binding sites in exons 2 and 3. These results suggest surprisingly high MHC diversity in knots, given their demographic history. This may be a result of selection from diverse pathogens encountered by shorebirds throughout their annual migrations.

Every year 50 million migratory waterbirds migrate from southern non-breeding areas in Southeast ... more Every year 50 million migratory waterbirds migrate from southern non-breeding areas in Southeast Asia and Australasia, to northern breeding grounds, mostly in Russia, but also in China, Mongolia, Japan, the Korean peninsula, and Alaska. The sum of these migration routes through 22 countries is defined as the East Asian-Australasian Flyway (EAAF). The EAAF is the most species-rich of the world’s nine major flyways. Unfortunately, the EAAF also has the highest proportion of declining waterbird populations. Waterbirds in the EAAF are in crisis. This report is an initiative for regional prioritization of the status of shorebird species using the EAAF, and is an objective assessment of the conservation status of EAAF populations using the latest available data on population size, trends, and distribution (e.g., endemism and use of sites), to determine which populations are most likely to reach or approach extinction if measures are not taken.

NIOZ rapport (ISSN, 1993

The Wageningen UR Library Catalogue contains bibliographic data on books and periodicals held by ... more The Wageningen UR Library Catalogue contains bibliographic data on books and periodicals held by the libraries of Wageningen University and Research Centre and some 15 associated libraries. Holding data are added to each record. ... Subjects covered include Agrotechnology, Food and Food Production, Plant and Animal Sciences, Soil Science, Geo-information, Landscape and Spatial Planning, Water and Climate, Ecosystem Studies, Economics and Society. ... The joint collections of the participating libraries cover a substantial part of ...

Ardea, Jan 1, 2010

Seasonal bird migration involves long flights, but most time is actually spent at intermediate st... more Seasonal bird migration involves long flights, but most time is actually spent at intermediate staging areas. The duration of stay at these sites can be evaluated with mark–recapture methods that employ day-to-day local encounters of individually marked birds. Estimates of staging duration are based on two probabilities: the immigration probability, the complement of a bird’s seniority to an area, and the emigration probability, the complement of the staying probability. Estimating total staging duration from seniority and staying probabilities requires validation for resighting data and here we compare three data categories of Ruffs Philomachus pugnax passing through The Netherlands during northward migration: (1) newly colour-ringed, (2) previously colour-ringed and (3) radio-tagged Ruffs (recorded by automated receiving stations). Between 2004 and 2008, 4363 resighting histories and 95 telemetry recording histories were collected. As sample sizes for females were low, only data for males were analysed. Possible catching effects affecting estimates of staging duration were explored. Staying probability was estimated for all data. Seniority however, could not be estimated for newly marked Ruffs; the assumption of equal ‘capture’ probability for reverse-time models applied to estimate seniority is violated for seasonal resighting histories starting with a catching event. Therefore, estimates of total staging duration were based on resightings of previously colourmarked birds only. For radio-tagged birds a minimal staging duration (time between tagging and last recording) was calculated. Modelling indicated that newly colour-ringed birds had a higher staying probability than previously colour-ringed birds, but the difference translated to a prolonged staging duration in newly ringed birds of only 0.4–0.5 d, suggesting a very small catching effect. The minimal staging duration of radio-tagged birds validated estimates of staging duration for colour-ringed birds in 2007 but not in 2005. In 2005 a low resighting probability resulted in underestimates of staging duration. We conclude that (1) estimates of staying probability can be affected by catching although effects on staging duration might be small, and that (2) low resighting probabilities can lead to underestimates in staging duration. In our study previously ringed Ruffs resighted in 2006–08 yielded reliable estimates of staging duration as data had sufficiently high resighting probabilities. Average staging durations varied between 19 d in 2008 and 23 d in 2006.

Molecular Phylogenetics and Evolution, Jan 1, 2010

Although the mitochondrial genome in birds has highly conserved features, with protein genes simi... more Although the mitochondrial genome in birds has highly conserved features, with protein genes similar to mammals and amphibians, several variations in gene order around the hypervariable control region have been found. Here we report a novel gene arrangement around the control region in shorebirds (Charadriiformes). In ruffs Philomachus pugnax, the mitochondrial genome between cytochrome b and 12SrRNA was over 1.5 kb longer than reported for other Charadriiformes and contained a duplication of the control region together with NADH dehydrogenase subunit 6 (ND6) and the adjacent transfer RNAs: tRNA(Pro) and tRNA(Glu). Sequence data from 68 individuals from several stopover and breeding populations show that the duplication is widespread in ruffs. Similar gene re-arrangements have been found independently in unrelated tube-nosed seabirds and spoonbills.

Molecular Ecology …, Jan 1, 2009

We isolated and tested 16 microsatellite loci in black-tailed godwits from the Netherlands (Limos... more We isolated and tested 16 microsatellite loci in black-tailed godwits from the Netherlands (Limosa limosa limosa), and from Australasia (subspecies melanuroides). One locus was
monomorphic, two loci had null-alleles and one was significantly heterozygote deficient. The remaining 12 polymorphic loci had on average 7.9 alleles (range 5–11) and the mean expected heterozygosity was 0.69. No significant linkage disequilibrium between the loci was observed and all loci were autosomal. Fourteen loci were successfully cross-amplified in bar-tailed godwit (Limosa lapponica).

Ruffs are migrant shorebirds of inland habitats. This thesis describes seasonal migration and cha... more Ruffs are migrant shorebirds of inland habitats. This thesis describes seasonal migration and changes in range occupation of ruffs, and presents a comparative analysis of the population genetics of ruffs and related shorebird species. Two hypotheses about shorebird evolution are addressed. Firstly, it is questioned whether instead of evolutionary constraints on migration routes (inflexible migration hypothesis), flexible routing might better explain observations on migration in shorebirds. Secondly, we test whether genetic variation in ruff and other inland, freshwater shorebirds is higher than in marine, coastal shorebirds (habitat dichotomy hypothesis).

… : progress report for …

Knowledge of stopover timing in migratory birds allows us to understand (1) a species’ migrating ... more Knowledge of stopover timing in migratory birds allows us to understand (1) a species’ migrating strategy and (2) the population dynamics at a particular stopover site along the flyway. The Ruff is an inland migratory shorebird, well studied for its reproductive behaviour but its migration is poorly known. We monitored turnover and population size during stopover in The Netherlands, by colour-marking and radio-tagging Ruffs individually. Using capture-recapture analysis, we estimated day to day survival, staging duration, staging numbers and new arrivals throughout the season. Our estimates revealed patterns not visible in normal census data.

Ringing & …, Jan 1, 2007

In spring, the Ruff Philomachus pugnax passes through European inland sites in large numbers. Bir... more In spring, the Ruff Philomachus pugnax passes through European inland sites in large numbers. Birds from eastern and western parts of the breeding range may differ in biometrics, but data on this species in eastern Europe are scarce. The aim of this study was to describe the biometrics of Ruffs migrating through southern Belarus in spring. In 2004, 242 birds were sexed by DNA analysis. Three birds sexed as males had female plumage but wing lengths intermediate between females and breeding-plumage males, and were identified as cryptic males or ‘faeders’. Between 2001 and 2005, 2,237 Ruffs were ringed at the study site (1,310 males in breeding plumage, 911 females and 14 faeders). There was a strong seasonal variation in sex ratio. For adult Ruffs wing length was the best predictor of sex. Total head length and tarsusplus-toe length distributions overlapped slightly between the sexes. There was evidence for slight bimodality in the distributions of wing, bill and tarsus-plus-toe length in non-faeder males and in wing and bill length distributions for females. Mean wing lengths of Ruffs passing through the Belarus study site were similar to those birds from other locations in Europe and North Africa, but different from birds from South Africa, Yamal and the middle Lena River, suggesting that Ruffs have at least two different breeding populations.