Friends or foes? Blood parasite costs and defence abilities in young raptor hosts

Rinaud T. Friends or foes? Blood parasite costs and defence abilities in young raptor hosts. Bielefeld: Universität Bielefeld; 2023.Short after coming to life, young vertebrates face many new challenges. How early-life adversity is dealt with during this critical developmental period primes a spectrum of long-term consequences for host fitness, that may ultimately regulate population dynamics. In this thesis, I intend to address aspects of this fundamental arc at increasing organizational scales, from gene, tissue, individual to population. I use multiple approaches such as transcriptomic, blood chemistry, physiology, and survival analyses, to assess host defence abilities and consequences of endoparasite infections during host nestling phase. I show that in a long-lived raptor, the common buzzard (Buteo buteo), nestlings infected with the blood parasite Leucocytozoon toddi display low transcriptional response to increasing parasitemia (density of parasite per host cells), moderate signs of parasite-induced tissue damages in the blood, disease symptoms only at the highest parasitemia level, and ultimately no effect of early-life infection on medium- to long-term survival. Additionally, through a combination of genotyping, whole genome and RNA sequencing we reveal that this nestling population presents a higher MHC allele diversity than previously thought. Antimalarial medication successfully reduced Leucocytozoon parasitemia in these young hosts but did not clear infections in most cases. Interestingly, treated nestlings did not show blood chemistry changes and physiological improvements compared with control nestlings. Altogether, this thesis emphasizes that Leucocytozoon parasites reside on the lower side of parasitic virulence spectrum. They appear to induce minor consequences to young long-lived hosts, at various organizational levels, although we show that nestlings already possess functional antiparasitic defences. This may provide the opportunity for growing hosts to rely on moderate defence responses, sometimes leading to disease symptoms during the harshest of infections and potentially impairing fitness of some particularly susceptible nestlings. Long-lived altricial nestlings and low-burden parasites may have co-evolved these traits, enabled by the naïve and immature host phase as a stable host-parasite evolutionary playground

High functional allelic diversity and copy number in both MHC classes in the common buzzard

Winternitz J, Chakarov N, Rinaud T, Ottensmann M, Krüger O. High functional allelic diversity and copy number in both MHC classes in the common buzzard. BMC Ecology and Evolution . 2023;23(1): 24.BACKGROUND: The major histocompatibility complex (MHC), which encodes molecules that recognize various pathogens and parasites and initiates the adaptive immune response in vertebrates, is renowned for its exceptional polymorphism and is a model of adaptive gene evolution. In birds, the number of MHC genes and sequence diversity varies greatly among taxa, believed due to evolutionary history and differential selection pressures. Earlier characterization studies and recent comparative studies suggest that non-passerine species have relatively few MHC gene copies compared to passerines. Additionally, comparative studies that have looked at partial MHC sequences have speculated that non-passerines have opposite patterns of selection on MHC class I (MHC-I) and class II (MHC-II) loci than passerines: namely, greater sequence diversity and signals of selection on MHC-II than MHC-I. However, new sequencing technology is revealing much greater MHC variation than previously expected while also facilitating full sequence variant detection directly from genomic data. Our study aims to take advantage of high-throughput sequencing methods to fully characterize both classes and domains of MHC of a non-passerine bird of prey, the common buzzard (Buteo buteo), to test predictions of MHC variation and differential selection on MHC classes.; RESULTS: Using genetic, genomic, and transcriptomic high-throughput sequencing data, we established common buzzards have at least three loci that produce functional alleles at both MHC classes. In total, we characterize 91 alleles from 113 common buzzard chicks for MHC-I exon 3 and 41 alleles from 125 chicks for MHC-IIB exon 2. Among these alleles, we found greater sequence polymorphism and stronger diversifying selection at MHC-IIB exon 2 than MHC-I exon 3, suggesting differential selection pressures on MHC classes. However, upon further investigation of the entire peptide-binding groove by including genomic data from MHC-I exon 2 and MHC-IIA exon 2, this turned out to be false. MHC-I exon 2 was as polymorphic as MHC-IIB exon 2 and MHC-IIA exon 2 was essentially invariant. Thus, comparisons between MHC-I and MHC-II that included both domains of the peptide-binding groove showed no differences in polymorphism nor diversifying selection between the classes. Nevertheless, selection analysis indicates balancing selection has been acting on common buzzard MHC and phylogenetic inference revealed that trans-species polymorphism is present between common buzzards and species separated for over 33 million years for class I and class II.; CONCLUSIONS: We characterize and confirm the functionality of unexpectedly high copy number and allelic diversity in both MHC classes of a bird of prey. While balancing selection is acting on both classes, there is no evidence of differential selection pressure on MHC classes in common buzzards and this result may hold more generally once more data for understudied MHC exons becomes available. © 2023. The Author(s)

High functional allelic diversity and copy number in both MHC classes in the common buzzard

Abstract Background The major histocompatibility complex (MHC), which encodes molecules that recognize various pathogens and parasites and initiates the adaptive immune response in vertebrates, is renowned for its exceptional polymorphism and is a model of adaptive gene evolution. In birds, the number of MHC genes and sequence diversity varies greatly among taxa, believed due to evolutionary history and differential selection pressures. Earlier characterization studies and recent comparative studies suggest that non-passerine species have relatively few MHC gene copies compared to passerines. Additionally, comparative studies that have looked at partial MHC sequences have speculated that non-passerines have opposite patterns of selection on MHC class I (MHC-I) and class II (MHC-II) loci than passerines: namely, greater sequence diversity and signals of selection on MHC-II than MHC-I. However, new sequencing technology is revealing much greater MHC variation than previously expected while also facilitating full sequence variant detection directly from genomic data. Our study aims to take advantage of high-throughput sequencing methods to fully characterize both classes and domains of MHC of a non-passerine bird of prey, the common buzzard (Buteo buteo), to test predictions of MHC variation and differential selection on MHC classes. Results Using genetic, genomic, and transcriptomic high-throughput sequencing data, we established common buzzards have at least three loci that produce functional alleles at both MHC classes. In total, we characterize 91 alleles from 113 common buzzard chicks for MHC-I exon 3 and 41 alleles from 125 chicks for MHC-IIB exon 2. Among these alleles, we found greater sequence polymorphism and stronger diversifying selection at MHC-IIB exon 2 than MHC-I exon 3, suggesting differential selection pressures on MHC classes. However, upon further investigation of the entire peptide-binding groove by including genomic data from MHC-I exon 2 and MHC-IIA exon 2, this turned out to be false. MHC-I exon 2 was as polymorphic as MHC-IIB exon 2 and MHC-IIA exon 2 was essentially invariant. Thus, comparisons between MHC-I and MHC-II that included both domains of the peptide-binding groove showed no differences in polymorphism nor diversifying selection between the classes. Nevertheless, selection analysis indicates balancing selection has been acting on common buzzard MHC and phylogenetic inference revealed that trans-species polymorphism is present between common buzzards and species separated for over 33 million years for class I and class II. Conclusions We characterize and confirm the functionality of unexpectedly high copy number and allelic diversity in both MHC classes of a bird of prey. While balancing selection is acting on both classes, there is no evidence of differential selection pressure on MHC classes in common buzzards and this result may hold more generally once more data for understudied MHC exons becomes available

Interspecific competition between two partridges in farmland landscapes

International audienceInterspecific competition is expected to occur between phylogenetically closely related species when sharing resources. In birds, interspecific competition often occurs by song-mediated interference and frequently implies asymmetrical outcomes between the species pairs involved. Habitat loss resulting from agricultural intensification is expected to have aggregated bird species in the remaining suitable habitats, thus increasing the likelihood of interspecific competition. However, this process has rarely been considered as a potential factor limiting population recovery in farmland birds. We investigated whether interspecific competition occurs between grey, Perdix perdix, and red-legged, Alectoris rufa, partridges, two phylogenetically related species. Originally parapatric, they have suffered an artificial increase in their contact zone due to huge human-mediated gamebird releases. We analysed territorial behaviour through a playback stimuli experiment and investigated shifts in habitat niche in the absence and presence of a hypothetical competitor. Results showed that the grey partridge appeared less territorial when co-occurring with the red-legged partridge and shifted its habitat niche away from the latter, while no such change was detected for the red-legged partridge. These asymmetrical patterns in behaviour and ecology are predicted under an interspecific competition scenario beneficial to the red-legged partridge, and therefore suggest that they are competitively dominant to grey partridges where they co-occur. This result has potentially strong implications for the management of grey partridges as gamebirds, and for their conservation in areas where they are almost extirpated

Tolerability of Atovaquone—Proguanil Application in Common Buzzard Nestlings

Wiegmann A, Rinaud T, Ottensmann M, et al. Tolerability of Atovaquone—Proguanil Application in Common Buzzard Nestlings. Veterinary Sciences. 2022;9(8): 397.Differences in drug tolerability among vertebrate groups and species can create substantial challenges for wildlife and ex situ conservation programmes. Knowledge of tolerance in the use of new drugs is, therefore, important to avoid severe toxicity in species, which are both commonly admitted in veterinary clinics and are of conservation concern. Antimalarial drugs have been developed for use in human medicine, but treatment with different agents has also long been used in avian medicine, as haemosporidian infections play a major role in many avian species. This study investigates the effects of the application of atovaquone–proguanil (Malarone®, GlaxoSmithKline) in common buzzards (Buteo buteo). The potential effects of treatment on body condition, growth rate, and chemical blood parameters of nestlings were assessed. All individuals survived the treatment, and no effects on body condition, growth rate, and chemical blood parameters were observed. Our results suggest the tolerability of Malarone® in common buzzards at a single dose of on average 11 mg/kg body weight. For its safe use, we recommend further studies to determine pharmacokinetics in different avian species as well as to assess the effects of repeated treatment

The prevalence of Leucocytozoon spp. in nestlings of three wild raptor species including implications on haematological and blood chemistry values

Wiegmann A, Springer A, Rinaud T, et al. The prevalence of Leucocytozoon spp. in nestlings of three wild raptor species including implications on haematological and blood chemistry values. International journal for parasitology. Parasites and wildlife. 2021;16:236-243.Leucocytozoonosis is a vector-borne infection of birds, caused by members of the haemosporidian genus Leucocytozoon. The clinical presentation may range from asymptomatic to severe disease. Consequences of Leucocytozoon infection on blood profiles remain to be described, especially for different host species in the wild. In the current study, the prevalence of Leucocytozoon infection was determined in wild nestlings of three European raptor species, the common buzzard (Buteo buteo, n=464), red kite (Milvus milvus, n=46) and northern goshawk (Accipiter gentilis, n=18). Among 528 nestlings, 51.9% (n=274) were infected with Leucocytozoon spp., whereby the highest prevalence was found in common buzzards (54.9%), followed by red kites (32.6%) and northern goshawks (22.2%). For a subset of 87 individuals (50 common buzzards, 29 red kites, 8 northern goshawks), a detailed analysis of differential leukocyte counts and several blood chemistry parameters in response to infection was conducted: AP (alkaline phosphatase), AST (aspartate aminotransferase), GLDH (glutamate dehydrogenase), LDH (lactate dehydrogenase), GGT (gamma glutamyl transferase), CK (creatine kinase), BuChE (butyrylcholinesterase), BA (bile acids), ALB (albumin) and TP (total protein). Even though in the physiological range, infected nestlings displayed significantly increased levels of heterophils, aspartate aminotransferase, lactate dehydrogenase, bile acids and butyrylcholinesterase, but decreased lymphocyte and monocyte values compared to uninfected ones. Furthermore, significant species differences with regard to blood parameters, but no sex differences were found. Overall, obtained results show a high prevalence, but a low pathogenicity of Leucocytozoon spp. in wild raptor chicks, presumably resulting from coevolutionary adaptation, but show signatures of infection in the haematological and blood chemistry profiles. © 2021 The Authors