Dermanyssus gallinae (de Geer) is an obligatory blood feeding ectoparasite (Chauve, 1998). Primarily a parasite of birds, most notably laying hens, D. gallinae demonstrates considerable plasticity regarding host specificity and is capable of feeding on mammals, including humans (Valiente Moro et al., 2009). Dermanyssus gallinae is reported to have a worldwide distribution with high percentages of laying hen farms affected in European countries including Denmark, France, Romania, Italy, the Netherlands, Poland, Serbia and the United Kingdom (UK) (Sparagano et al., 2014, Hoglund et al., 1995, Guy et al., 2004, Fiddes et al., 2005, Cencek, 2003). In the UK, for example, between 60% and 85% of commercial hen egg laying systems are reported to be infested (Guy et al., 2004, Fiddes et al., 2005). Dermanyssus gallinae causes significant economic losses to the European poultry industry, estimated at ~€231 million per annum (Van Emous, 2017) attributed to higher feed conversion ratios, reduced quality and number of eggs, and the cost of control (Sparagano et al., 2014). Losses in the UK alone were estimated at €3 million in 2008 (Sparagano et al., 2014) and infestation rates have increased significantly since then. Affected hens become restless and display signs of itching/irritation with severe infections causing anaemia which can, especially in young hens at point of lay, cause death (Marangi et al., 2009b). Research by Kilpinen et al. (2005) on the influence of D. gallinae infestation on laying hen health showed a reduction in weight gain in young hens when compared to hens without infestation that persisted for at least 100 days (Kilpinen et al., 2005). In addition to the direct impacts of infestation, it is suggested that D. gallinae plays a role in bird-to-bird transmission of other pathogens including some that are zoonotic. For example, Newcastle disease virus has been isolated from D. gallinae mites (Arzey, 1990) and it has been shown experimentally that D. gallinae is capable of transmitting Pasteurella multocida and Salmonella enterica enterica serovar Gallinarum between birds (Petrov, 1975, Cocciolo et al., 2020).
Control of D. gallinae most commonly relies on the use of various classes of chemical compounds collectively referred to as ‘acaricides’ (Sparagano et al., 2014), although widespread resistance to many current products has been demonstrated (Marangi et al., 2012, Katsavou et al., 2020, Marangi et al., 2009a). Dermanyssus gallinae infestation is increasingly common in Europe, its presence enhanced by bans on the use of some effective chemical treatments, as well as legislative changes that has seen traditional caged systems replaced by enriched cages whose more complex structures facilitate the survival and spread of mites (Sparagano et al., 2009). Novel control methods are urgently required to reduce the health, welfare and economic impacts of D. gallinae and this includes screening for novel drugs as well as research into the development of recombinant vaccines. Vaccination appears to be a feasible approach for controlling D. gallinae (Bartley et al., 2012, Wright et al., 2016, Bartley et al., 2017, Bartley et al., 2015) but optimal antigens and strategies for delivery are yet to be determined. Given the rapidity with which D. gallinae populations can become resistant to many acaricides, it is not clear how mite populations would respond to being targeted by recombinant vaccines or the rapidity with which immune escape may occur. Improving knowledge of population structures for D. gallinae including the extent of naturally occurring genetic diversity and potential for transmission of resistance/escape alleles will provide data to underpin future models of genome evolution in response to novel control strategies.
The importance of D. gallinae and opportunities offered by modern sequencing and genotyping platforms has seen recent increases in genetic studies and data in public databases. Studies of diversity have mainly focused on the cytochrome c oxidase subunit I (COI) coding sequence (Marangi et al., 2009b, Oines and Brannstrom, 2011, Chu et al., 2015b, Roy and Buronfosse, 2011, Karp-Tatham et al., 2020), 16S rDNA (Roy et al., 2009b, Roy et al., 2010), and the internal transcribed spacer (ITS) regions (Marangi et al., 2012, Oines and Brannstrom, 2011, Chu et al., 2015a, Roy et al., 2010, Brannstrom et al., 2008, Potenza et al., 2009) and provide evidence for inter- and intra-national migration of mite populations. Studies by Roy et al. (2009; 2010) on species specificity of the Dermanyssidae included several mite species and numerous isolates of D. gallinae from several European regions (Roy et al., 2009b, Roy et al., 2010). They reported intra-species variation rates of <9% in the COI gene and, in conjunction with further analysis, suggested that D. gallinae represents a complex of hybridized lineages, possibly species, from a total of 35 haplotypes (Roy et al., 2010). Research by Roy et al. has previously revealed that D. gallinae sensu lato represents a species complex, with a minimum of at least two cryptic species present (where a cryptic species can be defined as one that cannot be distinguished just by morphological features). They define two cryptic species: D. gallinae sensu stricto and D. gallinae L1, with the species having been recorded in poultry farm populations across the world but not in other avians (Roy and Buronfosse, 2011, Roy et al., 2010, Roy et al., 2009a). In 2014, the first next-generation sequence (NGS) dataset for D. gallinae was transcriptome data published (Schicht et al., 2014). Total RNA was extracted from an acaricide-susceptible D. gallinae strain maintained at the University of Veterinary Medicine Hannover, Institute for Parasitology. Synthesis of cDNA was completed using a pool of RNA extracted from male and female mites, including all developmental stages in starved and fed states, followed by Roche 454 sequencing. The final dataset consisted of 267,464 transcribed sequences (231,657 singletons, 56 contigs and 35,751 isotigs) (Schicht et al., 2014). More recently, Burgess et al. released a draft genome assembly of the D. gallinae genome in 2018 (Burgess et al., 2018). They extracted genomic DNA from adult female D. gallinae mites and freshly laid eggs (collected from a layer farm in Scotland, UK), before using a combination of sequencings from PacBio and Oxford Nanopore Technologies MinION to produce a final assembly of 7,171 contigs with an assembled genome size of 959 Mb (Burgess et al., 2018).
In this paper we used these published D. gallinae genomic and transcriptomic resources to identify a panel of high-quality SNPs with utility for genome-wide population genetic analyses. Using a Mid-Plex SNP genotyping assay we have assessed the occurrence and extent of genetic diversity in UK and other European D. gallinae populations, defining the occurrence of spatial and temporal variation.