Advancing mite phylogenomics: Designing ultraconserved elements for Acari phylogeny

Mites (Acari) are one of the most diverse groups of life on Earth; yet, their evolutionary relationships are poorly understood. Also, the resolution of broader arachnid phylogeny has been hindered by an underrepresentation of mite diversity in phylogenomic analyses. To further our understanding of Acari evolution, we design targeted ultraconserved genomic elements (UCEs) probes, intended for resolving the complex relationships between mite lineages and closely related arachnids. We then test our Acari UCE baits in‐silico by constructing a phylogeny using 13 existing Acari genomes, as well as 6 additional taxa from a variety of genomic sources. Our Acari‐specific probe kit improves the recovery of loci within mites over an existing general arachnid UCE probe set. Our initial phylogeny recovers the major mite lineages, yet finds mites to be non‐monophyletic overall, with Opiliones (harvestmen) and Ricinuleidae (hooded tickspiders) rendering Parasitiformes paraphyletic.     

A phylogenetic analysis of the arachnid orders based on morphological characters

Morphological evidence for resolving relationships among arachnid orders was surveyed and assembled in a matrix comprising 59 euchelicerate genera (41 extant, 18 fossil) and 202 binary and unordered multistate characters. Parsimony analysis of extant genera recovered a monophyletic Arachnida with the topology (Palpigradi (Acaromorpha (Tetrapulmonata (Haplocnemata, Stomothecata nom. nov. )))), with Acaromorpha containing Ricinulei and Acari, Tetrapulmonata containing Araneae and Pedipalpi (Amblypygi, Uropygi), Haplocnemata (Pseudoscorpiones, Solifugae) and Stomothecata (Scorpiones, Opiliones). However, nodal support and results from exploratory implied weights analysis indicated that relationships among the five clades were effectively unresolved. Analysis of extant and fossil genera recovered a clade, Pantetrapulmonata nom nov. , with the topology (Trigonotarbida (Araneae (Haptopoda (Pedipalpi)))). Arachnida was recovered as monophyletic with the internal relationships (Stomothecata (Palpigradi, Acaromorpha (Haplocnemata, Pantetrapulmonata))). Nodal support and exploratory implied weights indicated that relationships among these five clades were effectively unresolved. Thus, some interordinal relationships were strongly and/or consistently supported by morphology, but arachnid phylogeny is unresolved at its deepest levels. Alternative hypotheses proposed in the recent literature were evaluated by constraining analyses to recover hypothesized clades, an exercise that often resulted in the collapse of otherwise well-supported clades. These results suggest that attempts to resolve specific nodes based on individual characters, lists of similarities, evolutionary scenarios, etc., are problematic, as they ignore broader impacts on homoplasy and analytical effects on non-target nodes.  © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society , 2007, 150 , 221–265.     

A fossil trigonotarbid arachnid with a ricinuleid-like pedipalpal claw

A fossil trigonotarbid (Arachnida: Trigonotarbida) assigned to Palaeocharinus sp. from the Early Devonian (c. 410 Ma) Rhynie cherts of Aberdeenshire, Scotland, UK is described, specifically for a previously unrecognised feature of the distal end of the pedipalp. This exhibits a small chela formed from a movable, unpaired apotele articulating against a slightly shorter, fixed projection from the inferior surface of the tarsus. Among other arachnids, this morphology has only previously been observed in the rare and enigmatic Carboniferous—Recent taxon Ricinulei. This character offers explicit support for a monophylum (Trigonotarbida + Ricinulei); a hypothesis previously based on opisthosomal characters which (if correct) would draw Ricinulei within the so-called Pantetrapulmonata clade (i.e. spiders and their closest relatives). Our data is not consistent with Ricinulei’s traditional position as sister-group of mites (Acari) and is an example of how considering extinct taxa may help to resolve the position of a ‘difficult’ living group.     

Feather mites and birds: an interaction mediated by uropygial gland size?

Feather mites (Arachnida: Acari: Astigmata) feed mainly on secretions of the uropygial gland of birds. Here, we use analyses corrected for phylogeny and body size to show that there is a positive correlation between the size of this gland and mite abundance in passerine birds at an interspecific level during the breeding season, suggesting that the gland mediates interactions between mites and birds. As predicted on the basis of hypothesized waterproofing and antibiotic functions of uropygial gland secretions, riparian/marsh bird species had larger glands and higher mite loads than birds living in less mesic terrestrial environments. An unexpected pattern was a steeper relationship between mite load and gland size in migratory birds than in residents. If moderate mite loads are beneficial to a host but high loads detrimental, this could create complex selection regimes in which gland size influences mite load and vice versa. Mites may exert selective pressures on gland size of their hosts that has resulted in smaller glands among migratory bird species, suggesting that smaller glands may have evolved in these birds to attenuate a possible detrimental effect of feather mites when present in large numbers.     

Phylogenetic position of the acariform mites: sensitivity to homology assessment under total evidence

Background  

Mites (Acari) have traditionally been treated as monophyletic, albeit composed of two major lineages: Acariformes and Parasitiformes. Yet recent studies based on morphology, molecular data, or combinations thereof, have increasingly drawn their monophyly into question. Furthermore, the usually basal (molecular) position of one or both mite lineages among the chelicerates is in conflict to their morphology, and to the widely accepted view that mites are close relatives of Ricinulei.     

REVIEW Evolution and systematics of the Chelicerata

After approximately 40 years of discussion about the question of whether the Arthropoda are a monophyletic or a paraphyletic group or even a polyphyletic assemblage of unrelated taxa, most morphologists, palaeontologists and molecular taxonomists agree that the Arthropoda are a monophylum. The Euarthropoda are composed of the Arachnomorpha and Mandibulata. Myriapods are usually considered to be mandibulates; however, new molecular data as well as some morphological characters show similarities which the Myriapoda share with the Chelicerata, suggesting that there is no taxon Antennata or Atelocerata. Chelicerata are usually considered to be the sister group of Trilobita or, more correctly, Trilobita branch off from the chelicerate stem line. The first adaptive radiation of the Chelicerata took place in the Cambrian. All extant and some extinct orders were present during the Carboniferous. Two systems are compared. It is suggested that the Chelicerata contain the Pantopoda and Euchelicerata. The Euchelicerata are divided into Xiphosura and terrestrial Arachnida. Scorpiones are considered to be the sister group of all other arachnids, the Lipoctena and these are further divided into the Megoperculata (Uropygi, Amblypygi, and Araneae) and Apulmonata (all other groups). The Acari are tentatively considered to be a monophylum and the sister group of the Ricinulei. However, the Actinotrichida and Anactinotrichida diverged early and therefore have had a long history of independent evolution.     

“Jack‐of‐all‐trades” is parthenogenetic

Sex is evolutionarily more costly than parthenogenesis, evolutionary ecologists therefore wonder why sex is much more frequent than parthenogenesis in the majority of animal lineages. Intriguingly, parthenogenetic individuals and species are as common as or even more common than sexuals in some major and putative ancient animal lineages such as oribatid mites and rotifers. Here, we analyzed oribatid mites (Acari: Oribatida) as a model group because these mites are ancient (early Paleozoic), widely distributed around the globe, and include a high number of parthenogenetic species, which often co‐exist with sexual oribatid mite species. There is evidence that the reproductive mode is phylogenetically conserved in oribatid mites, which makes them an ideal model to test hypotheses on the relationship between reproductive mode and species'' ecological strategies. We used oribatid mites to test the frozen niche variation hypothesis; we hypothesized that parthenogenetic oribatid mites occupy narrow specialized ecological niches. We used the geographic range of species as a proxy for specialization as specialized species typically do have narrower geographic ranges than generalistic species. After correcting for phylogenetic signal in reproductive mode and demonstrating that geographic range size has no phylogenetic signal, we found that parthenogenetic lineages have a higher probability to have broader geographic ranges than sexual species arguing against the frozen niche variation hypothesis. Rather, the results suggest that parthenogenetic oribatid mite species are more generalistic than sexual species supporting the general‐purpose genotype hypothesis. The reason why parthenogenetic oribatid mite species are generalists with wide geographic range sizes might be that they are of ancient origin reflecting that they adapted to varying environmental conditions during evolutionary history. Overall, our findings indicate that parthenogenetic oribatid mite species possess a widely adapted general‐purpose genotype and therefore might be viewed as “Jack‐of‐all‐trades.”     

The embryogenesis of the Tick Rhipicephalus (Boophilus) microplus: The establishment of a new chelicerate model system

Summary: Chelicerates, which include spiders, ticks, mites, scorpions, and horseshoe crabs, are members of the phylum Arthropoda. In recent years, several molecular experimental studies of chelicerates have examined the embryology of spiders; however, the embryology of other groups, such as ticks (Acari: Parasitiformes), has been largely neglected. Ticks and mites are believed to constitute a monophyletic group, the Acari. Due to their blood‐sucking activities, ticks are also known to be vectors of several diseases. In this study, we analyzed the embryonic development of the cattle tick, Rhipicephalus (Boophilus) microplus (Acari: Ixodidae). First, we developed an embryonic staging system consisting of 14 embryonic stages. Second, histological analysis and antibody staining unexpectedly revealed the presence of a population of tick cells with similar characteristics to the spider cumulus. Cumulus cell populations also exist in other chelicerates; these cells are responsible for the breaking of radial symmetry through bone morphogenetic protein signaling. Third, it was determined that the posterior (opisthosomal) embryonic region of R. microplus is segmented. Finally, we identified the presence of a transient ventral midline furrow and the formation and regression of a fourth leg pair; these features may be regarded as hallmarks of late tick embryogenesis. Importantly, most of the aforementioned features are absent from mite embryos, suggesting that mites and ticks do not constitute a monophyletic group or that mites have lost these features. Taken together, our findings provide fundamental common ground for improving knowledge regarding tick embryonic development, thereby facilitating the establishment of a new chelicerate model system. genesis 51:803–818. © 2013 Wiley Periodicals, Inc.     

Ricoseius loxocheles,a phytoseiid mite that feeds on coffee leaf rust

One of the most important diseases of coffee plants is the coffee leaf rust fungus Hemileia vastatrix Berkeley and Broome (Uredinales). It can cause 30 % yield loss in some varieties of Coffea arabica (L.). Besides fungus, the coffee plants are attacked by phytophagous mites. The most common species is the coffee red mite, Oligonychus ilicis McGregor (Acari: Tetranychidae). Predatory mites of the Phytoseiidae family are well-known for their potential to control herbivorous mites and insects, but they can also develop and reproduce on various other food sources, such as plant pathogenic fungi. In a field survey, we found Ricoseius loxocheles (De Leon) (Acari: Phytoseiidae) on the necrotic areas caused by the coffee leaf rust fungus during the reproductive phase of the pathogen. We therefore assessed the development, survivorship and reproduction of R. loxocheles feeding on coffee leaf rust fungus and measured predation and oviposition of this phytoseiid having coffee red mite as prey under laboratory conditions. The mite fed, survived, developed and reproduced successfully on this pathogen but it was not able to prey on O. ilicis. Survival and oviposition with only prey were the same as without food. This phytoseiid mite does not really use O. ilicis as food. It is suggested that R. loxocheles is one phytoseiid that uses fungi as a main food source.     

The book lungs of Scorpiones and Tetrapulmonata (Chelicerata, Arachnida): evidence for homology and a single terrestrialisation event of a common arachnid ancestor

The question of whether Arachnida (Chelicerata) conquered terrestrial habitats only once or several times is controversial. The key group in this respect is the Scorpiones. Several authors claim that they became terrestrial independently of other arachnid lineages. This argumentation uses two lines of evidence. One is that book lungs of scorpions and other arachnids are considered non-homologous because they occur on different segments. The other line is based on fossil evidence which suggests that early scorpions were aquatic, together with a putative sister group relationship between scorpions and the aquatic Eurypterida. To address this problem we undertook a comparative scanning electron microscopical and histological study of the book lungs of scorpions, amblypygids, uropygids, and mesothelid spiders. In addition, we included the book gills of a xiphosuran. We found several detailed similarities in the book lungs shared by all arachnid taxa studied. Based on these findings we conclude that arachnid book lungs are homologous. Furthermore, we suggest that the apomorphic book lungs of arachnids indicate a single terrestrialisation event in the stem lineage leading to Arachnida.     

Morphology of locomotor appendages in Arachnida: evolutionary trends and phylogenetic implications

The morphological diversity of locomotor appendages in Arachnida is surveyed lo reconstruct phylogenetic relationships and discover evolutionary trends in form and function. The appendicular skeleton and musculature of representatives from the ten living arachnid orders ate described, and a system of homology is proposed. Character polarities are established through comparison with an outgroup. Limulus polyphemus Xiphosura). Cladistic analysis suggests that Arachnida is monophyletic and that absence of extensor muscles is a primitive condition. Extensors are primitively absent in Araneae. Amblypygi, Uropygi, Palpigradi, Ricinulei and Acari. Most similarities in the appendages of these orders are symplesiomorphic so that phylogenetic relationships among the ‘extensorless’ groups cannot be resolved solely on the basis of appendicular characters. Extensor muscles appear to have evolved once, and their presence is considered a synapomorphic feature of Opiliones, Scorpiones, Pseudoscorpiones and Solifugae. Solifugae lack extensors, but a parsimonious interpretation of other characters indicates that this is a secondary, derived condition. The phylogenetic relationships among these four orders are clarified by modifications of the patellotibial joint. Cladistic analysis indicates that Opiliones may be the sister group of the other three orders and that Scorpiones is the sister group of Pseudoscorpiones and Solifugae. Conclusions concerning phylogenetic relationships and evolutionary morphology presented here differ substantially from those of earlier studies on the locomotor appendages of Arachnida.     

Morphology of locomotor appendages in Arachnida: evolutionary trends and phylogenetic implications

The morphological diversity of locomotor appendages in Arachnida is surveyed lo reconstruct phylogenetic relationships and discover evolutionary trends in form and function. The appendicular skeleton and musculature of representatives from the ten living arachnid orders ate described, and a system of homology is proposed. Character polarities are established through comparison with an outgroup. Limulus polyphemus Xiphosura). Cladistic analysis suggests that Arachnida is monophyletic and that absence of extensor muscles is a primitive condition. Extensors are primitively absent in Araneae. Amblypygi, Uropygi, Palpigradi, Ricinulei and Acari. Most similarities in the appendages of these orders are symplesiomorphic so that phylogenetic relationships among the 'extensorless' groups cannot be resolved solely on the basis of appendicular characters. Extensor muscles appear to have evolved once, and their presence is considered a synapomorphic feature of Opiliones, Scorpiones, Pseudoscorpiones and Solifugae. Solifugae lack extensors, but a parsimonious interpretation of other characters indicates that this is a secondary, derived condition. The phylogenetic relationships among these four orders are clarified by modifications of the patellotibial joint. Cladistic analysis indicates that Opiliones may be the sister group of the other three orders and that Scorpiones is the sister group of Pseudoscorpiones and Solifugae. Conclusions concerning phylogenetic relationships and evolutionary morphology presented here differ substantially from those of earlier studies on the locomotor appendages of Arachnida.     

Arrestment response of the predatory mite Amblyseius longispinosus to Schizotetranychus nanjingensis webnests on bamboo leaves (Acari: Phytoseiidae, Tetranychidae)

The response of the predatory mite Amblyseius longispinosus (Acari: Phytoseiidae) to the webnest of the spider mite nanjingensis (Acari: Tetranychidae) was examined using two-choice tests in the laboratory. A. longispinosus females were found significantly more often on leaves with webnests than on leaves without webnests and were often observed searching under the webbing. Because spider mites and their eggs were removed from the webnests before experiments, predators responded to stimuli associated with webbing, mite feeding damage and other residues in the webnests.     

Fine structure of the male genital system of the predatory mite Rhagidia halophila (Rhagidiidae,Prostigmata, Actinotrichida)

The male genital system of the actinotrichid mite Rhagidia halophila is described and compared with other mites and arachnids. The large testes are composed of germinal and glandular parts and produce numerous small sperm cells. The glandular parts are connected via a testicular bridge. Spermiogenesis occurs in cysts containing spermatids in equal stages of development. Cysts of spermatids are embedded in huge somatic cells. The nuclei of the spermatids loose their envelope. Mature sperm cells are simple exhibiting a ring‐shaped chromatin body and lacking an acrosomal complex. They are most similar to the sperm cells of the related mite Linopodes motatorius. The spermatopositor contains the ejaculatory duct divided into a dorsal channel and a ventral channel that are connected via a narrow passage. At its distal end, the spermatopositor is divided into three eugenital lips. The function of the spermatopositor during deposition of the peculiar thread‐like spermatophores is discussed. Details of the sensilla of the spermatopositor and the progenital lips are reported. The genital papillae located on the inner side of the progenital lips exhibit characteristics of cells performing transport of ions and/or water. The results confirm the overall similarity of actinotrichid genital systems, which is profoundly different from that of anactinotrichid mites. With reference to other Arachnida it is corroborated that testes and sperm structure of Actinotrichida are most similar to that of Solifugae. However, synapomorphies between sperm cells of Rhagidia and Solifugae that could suggest a closer relationship between these two taxa as was suggested in earlier studies were not recognizable. On the contrary, the sperm cells of Rh. halophila being devoid of an acrosomal complex appeared to be more apomorphic than those of many other actinotrichid mites as well as Solifugae. J. Morphol. 276:832–859, 2015. © 2015 Wiley Periodicals, Inc.     

Multiple convergent evolution of arboreal life in oribatid mites indicates the primacy of ecology

Frequent convergent evolution in phylogenetically unrelated taxa points to the importance of ecological factors during evolution, whereas convergent evolution in closely related taxa indicates the importance of favourable pre-existing characters (pre-adaptations). We investigated the transitions to arboreal life in oribatid mites (Oribatida, Acari), a group of mostly soil-living arthropods. We evaluated which general force—ecological factors, historical constraints or chance—was dominant in the evolution of arboreal life in oribatid mites. A phylogenetic study of 51 oribatid mite species and four outgroup taxa, using the ribosomal 18S rDNA region, indicates that arboreal life evolved at least 15 times independently. Arboreal oribatid mite species are not randomly distributed in the phylogenetic tree, but are concentrated among strongly sclerotized, sexual and evolutionary younger taxa. They convergently evolved a capitate sensillus, an anemoreceptor that either precludes overstimulation in the exposed bark habitat or functions as a gravity receptor. Sexual reproduction and strong sclerotization were important pre-adaptations for colonizing the bark of trees that facilitated the exploitation of living resources (e.g. lichens) and served as predator defence, respectively. Overall, our results indicate that ecological factors are most important for the observed pattern of convergent evolution of arboreal life in oribatid mites, supporting an adaptationist view of evolution.     

Do parasitic flies attack mites? Evidence in Baltic amber

We provide the first evidence of a small-headed fly planidium (first instar larva; Diptera: Acroceridae) associated with a whirligig mite (Acari: Acariformes: Prostigmata: Anystina: Anystidae) in Baltic amber. This fossil is surprising as parasitic nematodes are the only metazoans known to successfully attack acariform mites, and Acroceridae are believed to be host-restricted parasitoids of spiders. The fossil corroborates a previously published, but widely dismissed, paper that first reported parasitism of parasitengone mites by acrocerid planidia. The possible natural history implications of this find are discussed.  © 2008 The Linnean Society of London, Biological Journal of the Linnean Society , 2008, 93 , 9–13.     

A molecular‐genetic understanding of diapause in spider mites: current knowledge and future directions

During unfavourable conditions, many arthropods have the ability to enter into diapause and synchronize their development and reproduction to seasonal patterns. Diapause or winter hibernation in insects and mites is set off by a number of cues, with photoperiod being the most well‐defined and strongest signal. This review focuses on the current knowledge of ‘‐omics’ data and the genetics of diapause in the two‐spotted spider mite Tetranychus urticae, a member of the family Tetranychidae (Arthropoda: Chelicerata: Arachnida: Acari). This species is a serious polyphagous pest and females undergo a reproductive facultative diapause when immature stages are exposed to long nights. Winter hibernation induces different physiological processes characterized by a metabolic suppression, different energy use, increased stress tolerance and the production of cryoprotectants, all initiated by a complex signal transduction pathway. Keto‐carotenoids are known to cause the deeply orange colour typical for diapausing females. Furthermore, research with colour mutants of T. urticae has shown the need for carotenoids with respect to the induction of diapause, even though the molecular‐genetic mechanisms underlying these colour phenotypes are still unknown. In addition, marked latitudinal variation in diapause incidence among populations has been observed in nature, with modes of inheritance ranging from recessive to dominant, as well as monogenic to polygenic. We end by highlighting the emerging opportunities for functional studies that aim to unravel the complex factors underlying diapause in spider mites.     

Spatial distribution and abundance of bud galls caused by eriophyoid mites among host trees Carpinus tschonoskii

Abstract:  Differences in spatial distribution and abundance of bud galls caused by eriophyoid mites (Acari: Eriophyoidea) among Carpinus tschonoskii (Betulaceae) were studied. This mite preferentially induces galls on terminal buds. Four factors influencing gall abundance were examined: host tree size, host tree's reproductive status, altitude and study site. As tree size increased, the number of galls increased to an apparent asymptote. This result suggests that tree size-dependent characteristics such as number of terminal buds, temporal pattern of shoot elongation and reproductive status influence gall abundance.     

Guanine as a hygienic index for allergologically relevant mite infestations in mattress dust

Since guanine is not only an essential constituent of vital nucleic acids, but also the main end product of nitrogenous waste excretion in arachnids, it is a potential candidate for a hygienic index for mite activity in house dust. The public health significance of these mites is based on their production of allergen in the home environment.In 101 mattress-dust samples, total number of mites and guanine content were positively correlated. The hygienic standard of 10 mites per 0.1 g dust (as derived from Danish investigations) was met in all samples with less than 0.06% guanine in the dry dust. Where the guanine content was more than or equal to 0.25% in the dry dust, mite numbers were higher than 10 mites per 0.1 g dust in 43 of the 44 samples. The three different groups (negligible mite content, possibly allergologically relevant mite concentration and allergologically unhygienic mite situation) could be easily discriminated on the color scale.The guanine-AZO-dye reaction in vacuum cleaner dust is a strong and promising candidate for an allergologically relevant hygienic index in the home.