Andrew Dixon

Peregrine and saker falcon genome sequences provide insights into evolution of a predatory lifestyle

As top predators, falcons possess unique morphological, physiological and behavioral adaptations that allow them to be successful hunters: for example, the peregrine is renowned as the worlds fastest animal. To examine the evolutionary basis of predatory adaptations, we sequenced the genomes of both the peregrine (Falco peregrinus) and saker falcon (Falco cherrug), and we present parallel, genome-wide evidence for evolutionary innovation and selection for a predatory lifestyle. The genomes, assembled using Illumina deep sequencing with greater than 100-fold coverage, are both approximately 1.2 Gb in length, with transcriptome-assisted prediction of approximately 16,200 genes for both species. Analysis of 8,424 orthologs in both falcons, chicken, zebra finch and turkey identified consistent evidence for genome-wide rapid evolution in these raptors. SNP-based inference showed contrasting recent demographic trajectories for the two falcons, and gene-based analysis highlighted falcon-specific evolutionary novelties for beak development and olfaction and specifically for homeostasis-related genes in the arid environment–adapted saker.

The problem of raptor electrocution in Asia: case studies from Mongolia and China

We report a large number of raptors electrocuted on recently erected electricity distribution lines in the open landscapes of the Mongolian steppe and Qinghai-Tibetan plateau, China. Upland Buzzards Buteo hemilasius and Saker Falcons Falco cherrug , characteristic raptors of these bioregions, were among those found to be electrocuted. Raptor electrocution was a consequence of poorly designed hardware configurations on anchor poles along surveyed lines on the Qinghai-Tibetan Plateau and, additionally, on line poles in the Mongolian steppe. The design flaws were upright pin-insulators on earthed crossarms and the use of jump wires that passed over crossarms via pin insulators on anchor poles. Targeted mitigation of anchor poles could significantly reduce the incidence of electrocution on the lines surveyed on the Qinghai-Tibetan Plateau, whilst all poles on the lines surveyed in the Mongolian steppe require remediation to make them safe for raptors. The Mongolian steppe and the Qinghai-Tibetan Plateau are bioregions that hold the largest breeding and wintering populations of the globally threatened Saker Falcon. The existing and growing network of dangerous electricity distribution lines in these regions may potentially impact the Saker Falcon population, thus we suggest that preventative and/or mitigation measures are implemented.

Exonic versus intronic SNPs: contrasting roles in revealing the population genetic differentiation of a widespread bird species

Recent years have seen considerable progress in applying single nucleotide polymorphisms (SNPs) to population genetics studies. However, relatively few have attempted to use them to study the genetic differentiation of wild bird populations and none have examined possible differences of exonic and intronic SNPs in these studies. Here, using 144 SNPs, we examined population genetic differentiation in the saker falcon (Falco cherrug) across Eurasia. The position of each SNP was verified using the recently sequenced saker genome with 108 SNPs positioned within the introns of 10 fragments and 36 SNPs in the exons of six genes, comprising MHC, MC1R and four others. In contrast to intronic SNPs, both Bayesian clustering and principal component analyses using exonic SNPs consistently revealed two genetic clusters, within which the least admixed individuals were found in Europe/central Asia and Qinghai (China), respectively. Pairwise D analysis for exonic SNPs showed that the two populations were significantly differentiated and between the two clusters the frequencies of five SNP markers were inferred to be influenced by selection. Central Eurasian populations clustered in as intermediate between the two main groups, consistent with their geographic position. But the westernmost populations of central Europe showed evidence of demographic isolation. Our work highlights the importance of functional exonic SNPs for studying population genetic pattern in a widespread avian species.

Missense SNP of the MC1R gene is associated with plumage variation in the Gyrfalcon (Falco rusticolus)

A single nucleotide polymorphism (MC1R: c.376A>G) in the MC1R gene was found to be highly correlated with pigment phenotype in the Gyrfalcon. Homozygous genotypes c.376GG and c.376AA were found to dominate the extreme white and dark plumage types respectively, and heterozygotes occurred mainly in intermediate phenotypes. However, some heterozygotes were associated with extreme phenotypes, indicating that melanism/albinism might also involve other loci.

The potential use of artificial nests for the management and sustainable utilization of saker falcons (Falco cherrug)

AbstractArtificial nests are a commonly used management technique to increase the breeding population and/or productivity of birds with nest site limited populations. We compared nest survival of saker falcons breeding in artificial nests erected in a flat steppe landscape with those breeding in natural nests on rocks and cliffs in adjacent hills of central Mongolia. We found no significant difference in daily nest survival during the egg and nestling stages of the breeding cycle. Nest survival varied across years and was higher at artificial than natural nest sites, primarily because of higher survival rates during the egg stage at artificial nests. However, fledgling productivity was not significantly different although artificial nests produced an average of 3.2 fledglings compared to 2.3 at natural nest sites. We found no significant differences in offspring sex ratios and fledgling mass at artificial and natural nest sites. Provision of artificial nests can increase the range, size and productivity of saker falcon breeding populations, a globally endangered species subject to high mortality and trapping for falconry. This management technique can be used for incentive-driven conservation initiatives, whereby sustainable harvest quotas can be generated from demographic models based on parameters derived from a managed and monitored population breeding in artificial nests.ZusammenfassungDer mögliche Einsatz von Kunstnestern für das Management und die nachhaltige Nutzung von Sakerfalken (Falco cherrug) Kunstnester werden häufig beim Artenmanagement eingesetzt, um die Brutpopulation und/oder die Produktivität von Vögeln mit limitierten Nistplätzen zu steigern. Wir haben in der zentralen Mongolei das Überleben der Nester von Sakerfalken, die in Kunstnestern in flachen Steppenlandschaften brüteten, mit dem von in natürlichen Nestern auf Felsen und Klippen in angrenzenden Hügeln brütenden Falken verglichen. Wir fanden keinen signifikanten Unterschied im täglichen Überleben des Nests während der Bebrütungs- und Nestlingsphase. Das Nestüberleben unterschied sich zwischen verschiedenen Jahren und war an künstlichen Nistplätzen höher als an natürlichen, hauptsächlich da Kunstnester höhere Überlebensraten während des Bebrütungsstadiums aufwiesen. Die Flügglingsproduktion unterschied sich jedoch nicht signifikant, obwohl Kunstnester im Durchschnitt 3,2 Flügglinge produzierten und natürliche Nester nur 2,3. Wir fanden zwischen Kunst- und Naturnestern keine signifikanten Unterschiede im Geschlechterverhältnis der Nestlinge und in der Körpermasse der Flügglinge. Die Bereitstellung von Kunstnestern kann Verbreitung, Größe und Produktivität von Brutpopulationen des Sakerfalken erhöhen, einer global gefährdeten Art, die hohe Mortalität aufweist und für die Falknerei gefangen wird. Diese Managementmethode kann für anreizgetriebene Schutzinitiativen verwendet werden, wobei nachhaltige „Erntequoten“anhand von demographischen Modellen errechnet werden können, die auf Parametern basieren, welche von einer gemanagten und überwachten in Kunstnestern brütenden Population abgeleitet sind.

Population transcriptomes reveal synergistic responses of DNA polymorphism and RNA expression to extreme environments on the Qinghai-Tibetan Plateau in a predatory bird

Low oxygen and temperature pose key physiological challenges for endotherms living on the Qinghai–Tibetan Plateau (QTP). Molecular adaptations to high‐altitude living have been detected in the genomes of Tibetans, their domesticated animals and a few wild species, but the contribution of transcriptional variation to altitudinal adaptation remains to be determined. Here we studied a top QTP predator, the saker falcon, and analysed how the transcriptome has become modified to cope with the stresses of hypoxia and hypothermia. Using a hierarchical design to study saker populations inhabiting grassland, steppe/desert and highland across Eurasia, we found that the QTP population is already distinct despite having colonized the Plateau <2000 years ago. Selection signals are limited at the cDNA level, but of only seventeen genes identified, three function in hypoxia and four in immune response. Our results show a significant role for RNA transcription: 50% of upregulated transcription factors were related to hypoxia responses, differentiated modules were significantly enriched for oxygen transport, and importantly, divergent EPAS1 functional variants with a refined co‐expression network were identified. Conservative gene expression and relaxed immune gene variation may further reflect adaptation to hypothermia. Our results exemplify synergistic responses between DNA polymorphism and RNA expression diversity in coping with common stresses, underpinning the successful rapid colonization of a top predator onto the QTP. Importantly, molecular mechanisms underpinning highland adaptation involve relatively few genes, but are nonetheless more complex than previously thought and involve fine‐tuned transcriptional responses and genomic adaptation.

The Use of Power Lines by Breeding Raptors and Corvids in Mongolia: Nest-Site Characteristics and Management Using Artificial Nests

Abstract The use of power line support structures as nesting sites enables some raptors and corvids to increase their breeding range and/or density in landscapes where alternative nest sites are limited. We report on the use of power poles for nesting by two nest-building species, Common Raven (Corvus corax) and Upland Buzzard (Buteo hemilasius), and two falcon species, Saker Falcon (Falco cherrug) and Eurasian Kestrel (Falco tinnunculus) in the nest-site-limited steppes of central Mongolia. Various power pole designs differed in their attractiveness to nest-building species, with structures that provided stable support and shelter being significantly favored. Trials of artificial nest barrels to (i) provide alternative nest sites on favored nesting support structures and (ii) provide additional nest sites on unfavored support structures, failed to induce nest-building species to shift their nest location in the first instance or to increase overall breeding density of large raptors and corvids in the second case. However, both trials resulted in large increases in the number of nesting Eurasian Kestrels. USO DE TENDIDOS ELÉCTRICOS POR RAPACES REPRODUCTIVAS Y CÓRVIDOS EN MONGOLIA: CARACTERÍSTICAS DEL SITIO DE ANIDAMIENTO Y MANEJO UTILIZANDO NIDOS ARTIFICIALES El uso de las estructuras de soporte de los tendidos eléctricos como sitios de anidamiento permite a algunas rapaces y córvidos incrementar su área de reproducción y/o densidad en paisajes donde los sitios de anidamiento alternativos son limitados. Informamos el uso de postes de electricidad para anidar por parte de dos especies constructoras de nido, Corvus corax y Buteo hemilasius, y dos especies de halcones, Falco cherrug y Falco tinnunculus, en las estepas con sitios de anidamiento limitados del centro de Mongolia. Varios diseños de postes de electricidad difirieron en su atractivo para las especies constructoras de nidos, con una preferencia significativa por estructuras que proveen de un soporte estable y refugio. Los intentos de anidación en sitios artificiales, que implican (i) proveer sitios de anidamiento alternativos en estructuras de soporte preferidas para el anidamiento y (ii) proveer sitios de anidamiento adicionales en estructuras de soporte desfavorecidas, fallaron en el intento de inducir a las especies constructoras de nidos de cambiar la ubicación de sus nidos en primera instancia o en incrementar la densidad reproductiva total de rapaces grandes y córvidos en el segundo caso. Sin embargo, ambos intentos resultaron en grandes aumentos en el número de individuos anidando de F. tinnunculus.

Evidence for deleterious effects of harness-mounted satellite transmitters on Saker Falcons Falco cherrug

Capsule This study identifies lethal and sub-lethal effects associated with the deployment of harness-mounted satellite transmitters on a large falcon species. Aims We examined the effect of harness-mounted satellite transmitters and patagial tags on survival, behaviour and physical health of adult Saker Falcons. Methods We compared breeding turnover of Saker Falcons deployed with harness-mounted satellite transmitters or patagial tags with unmarked birds identified by using genetic markers. In addition, observational data were recorded on the breeding behaviour and physical condition of birds with satellite transmitters. Results This study found evidence of decreased survival, together with sub-lethal behavioural and physical effects, associated with the deployment of harness-mounted satellite transmitters on Saker Falcons. We found no effect of fitting patagial tags on breeding turnover, although the removal of patagial tags by several birds may have indicated they caused some degree of discomfort. Conclusion Researchers using harness-mounted transmitters on this, and similar, falcon species need to assess how these deleterious effects may impact on species conservation, the welfare of individual birds and the interpretation of their studies.

Population status of breeding Saker Falcons (Falco cherrug) in Turkey.

The Saker Falcon Falco cherrug breeds in Turkey and also occurs in the country during passage and in winter. Turkey represents the southwestern range limit of the global breeding distribution of the species and is relatively isolated from the neighbouring population centres in Europe and Central Asia. A review of literature and other record sources indicated that the 19th century breeding population in Thrace had disappeared by the 1950s, in line with dramatic declines in the Southern Balkans. We could find no data on the Saker Falcon population elsewhere in Turkey prior to the 1960s. In the 1960s, the Saker Falcon was a rare breeding species found mainly in steppe habitats of Central and Eastern Anatolia. Despite increased ornithological recording activity in the country, the number of Saker Falcon records declined in the 1980s and 1990s, probably because of habitat loss, a reduction in the Anatolian Souslik (Spermophilus xanthoprymnus) population and the activities of falcon trappers. A recent resurgence in records since 2000 probably reflects an increase in ornithological recording by resident and visiting ornithologists. Our survey in 2007 confirmed that the Saker is a rare breeding species in Central and Eastern Anatolia despite there being much apparently suitable habitat and prey available in these regions. It is not clear whether or not the Saker population in Turkey is currently held at a low level by anthropogenic factors or whether the low population size is a characteristic of an isolated population of a species occurring at the edge its global distribution range.

Integrated tool for microsatellite isolation and validation from the reference genome and their application in the study of breeding turnover in an endangered avian population

Accurate individual identification is required to estimate survival rates in avian populations. For endangered species, non-invasive methods of obtaining individual identification, such as using molted feathers as a source of DNA for microsatellite markers, are preferred because of less disturbance, easy sample preparation and high efficiency. With the availability of many avian genomes, a few pipelines isolating genome-wide microsatellites have been published, but it is still a challenge to isolate microsatellites from the reference genome efficiently. Here, we have developed an integrated tool comprising a bioinformatic pipeline and experimental procedures for microsatellite isolation and validation based on the reference genome. We have identified over 95 000 microsatellite loci and established a system comprising 10 highly polymorphic markers (PIC value: 0.49-0.93, mean: 0.79) for an endangered species, saker falcon (Falco cherrug). These markers (except 1) were successfully amplified in 126 molted feathers, exhibiting high amplification success rates (83.9-99.7%), high quality index (0.90-0.97) and low allelic dropout rates (1-9.5%). To further assess the efficiency of this marker system in a population study, we identified individual sakers using these molted feathers (adult) and 146 plucked feathers (offspring). The use of parent and offspring samples enabled us to infer the genotype of missing samples (N = 28), and all adult genotypes were used to ascertain that breeding turnover is a useful proxy for survival estimation in sakers. Our study presents a cost-effective tool for microsatellite isolation based on publicly available reference genomes and demonstrates the power of this tool in estimating key parameters of avian population dynamics.