Cryptic diversity within grass-associated Abacarus species complex (Acariformes: Eriophyidae), with the description of a new species, Abacarus plumiger n. sp.

Experimental and Applied Acarology https://doi.org/10.1007/s10493-018-0291-6 Cryptic diversity within grass‑associated Abacarus species complex (Acariformes: Eriophyidae), with the description of a new species, Abacarus plumiger n. sp. Alicja Laska1 · Agnieszka Majer1 · Wiktoria Szydło2 · Kamila Karpicka‑Ignatowska1 · Marta Hornyák3 · Anna Labrzycka4 · Anna Skoracka1 Received: 31 May 2018 / Accepted: 24 August 2018 © The Author(s) 2018 Abstract Accurate estimation of species richness is often complex as genetic divergence is not always accompanied by appreciable morphological differentiation. In consequence, cryptic lineages or species evolve. Cryptic speciation is common especially in taxa characterized by small and simplified bodies, what makes their proper identification challenging. The cereal rust mite, Abacarus hystrix, was regarded for a long time as a species associated with a wide range of grass hosts, whereas wide host ranges are rather rare in eriophyoid mites. Therefore, the generalist status of A. hystrix was questioned. In this paper we demonstrate that the diversity within Abacarus species associated with grasses is more complex than it was previously thought. The 78 Abacarus mtDNA COI sequences used in this study formed 10 highly supported clades (bootstrap value 99%) and four more distinct genetic lineages were represented by unique sequences. The genetic distances between them ranged from 6.6 to 26.5%. Moreover, morphological study and genetic approach based on the combination of the Poisson Tree Processes model for species delimitation (PTP) and a Bayesian implementation of PTP (bPTP), and Neighbour Joining analyses led to delimitation of a new species within the Abacarus complex: Abacarus plumiger, specialized on smooth brome (Bromus inermis). Furthermore, our analyses demonstrated a pattern of host-associated differentiation within the complex. Overall, our study indicates that cryptic speciation occurs in the grass-associated Abacarus genus, and suggests the need for more extensive sampling using integrative methods. Keywords Barcoding · Biodiversity · Cryptic species · Eriophyoid mites · mtDNA COI · Taxonomy * Alicja Laska Extended author information available on the last page of the article 13 Vol.:(0123456789) Experimental and Applied Acarology Introduction The genetic divergence leading to speciation is not always accompanied by appreciable morphological differentiation. In consequence, cryptic lineages or species evolve and their occurrence, being often overlooked, contributes to the underestimation of species richness (Gerhardt 2005; Stuart et al. 2006; Bickford et al. 2007; Pfenninger and Schwenk 2007; Ceballos and Ehrlich 2009; Wan et al. 2014) and although cryptic species are widespread and common, the magnitude of cryptic diversity remains unknown (Bickford et al. 2007; Pfenninger and Schwenk 2007; Stork 2018). Recognition of the extent of hidden diversity within any taxonomic group is essential to assess its overall diversity and to understand the complexity of its ecological interactions and evolutionary histories (Bickford et al. 2007; Skoracka et al. 2015). Furthermore, evaluation of cryptic diversity is of special importance for conservation biology, as well as for research on parasites and agricultural pests (Liu et al. 2012; Poulin 2014). Over the last 30 years, there has been an exponential increase in the number of studies that demonstrated the existence of cryptic diversity (Bickford et al. 2007; Poulin 2014; Espíndola et al. 2016; Živković et al. 2017). This rising trend is linked to increasing access to wide array of technologies that enable effective species delimitation. For example, employing super-resolution microscopy, such as electron or confocal microscopy, resulted in the deeper examination of morphology and ultrastructure details that could not be done with classical light microscopy (Chetverikov et al. 2013). Furthermore, increased access to molecular biology techniques had led to the development of barcoding procedures, which allowed fast species delimitation and discrimination on the genetic basis. As a result, many species that were initially described with traditional morphology-based methods as single taxonomic units, were later revealed to be complexes of cryptic species (Knowlton 1993; Funk et al. 2012; Skoracka et al. 2015). However, many of them, before correct identification with aid of genetic methods, had been suspected to be species complexes on the basis of their biological and ecological features (Henry and Wells 2010; Nygren et al. 2010; Skoracka and Dabert 2010). Cryptic species are prevalent in taxa which are microscopic in size and have simplified bodies (Skoracka et al. 2015), and these characteristics may hinder their proper identification based on morphological techniques that are prevalent in taxonomy (de Lillo et al. 2010; Zhao et al. 2013; Stork 2018). Eriophyoid mites are characterized by their minute size and simplified body structure, and their accurate identification by morphological traits is demanding (Lindquist 1996). However, nowadays taxonomist are integrating the traditional morphology approach with molecular tools to discriminate between species and to describe new species (e.g., Chetverikov et al. 2013; de Lillo et al. 2018). This is especially important in basic and applied studies of economically important cryptic species, which may differ, for example, in capacity for pathogen transmission or pesticide resistance (Pan et al. 2011; Miller et al. 2012). Eriophyoid mites are obligatory phytophagous arthropods and are highly specialized to their hosts. They are known as significant plant pests worldwide, that cause either direct damage to their host plant or transmit plant viruses. Recent research suggests that cryptic diversity may be very common in eriophyoid mites. It was demonstrated that the grass-associated wheat curl mite (WCM), Aceria tosichella Keifer, Brassicaceae-associated Aceria mites, and coniferous-associated Trisetacus mites are complexes that consist of divergent lineages which probably are cryptic species (Skoracka et al. 2012; Lewandowski et al. 2014; Živković et al. 2017). 13 Experimental and Applied Acarology An intensively studied example of cryptic diversity in eriophyoid mites is the cereal rust mite, Abacarus hystrix Nalepa, that long has been regarded as a single species adapted to numerous Poaceae species, with a wide host range including both cultivated and wild grasses—e.g., Triticum aestivum L. (wheat), Secale cereale L. (rye), Oryza sativa L. (rice), Cynodon dactylon L. (Bermuda grass), Lolium perenne L. (perennial ryegrass), Bromus inermis Leyss. (smooth brome), Bromus hordeaceus L. (soft brome), Bromus erectus Huds. (meadow brome), Dactylis glomerata L. (cocksfoot grass) (Frost and Ridland 1996). Abacarus hystrix has been recognized as a common pest of cereal fields and grasslands in Eurasia, North America, temperate regions of Africa (...truncated)