Cryptic speciation in the Acari: a function of species lifestyles or our ability to separate species?

Exp Appl Acarol (2015) 67:165–182 DOI 10.1007/s10493-015-9954-8 REVIEW PAPER Cryptic speciation in the Acari: a function of species lifestyles or our ability to separate species? Anna Skoracka1 • Sara Magalhães2 • Brian G. Rector3 • Lechosław Kuczyński4 Received: 10 March 2015 / Accepted: 19 July 2015 / Published online: 26 July 2015 Ó The Author(s) 2015. This article is published with open access at Springerlink.com Abstract There are approximately 55,000 described Acari species, accounting for almost half of all known Arachnida species, but total estimated Acari diversity is reckoned to be far greater. One important source of currently hidden Acari diversity is cryptic speciation, which poses challenges to taxonomists documenting biodiversity assessment as well as to researchers in medicine and agriculture. In this review, we revisit the subject of biodiversity in the Acari and investigate what is currently known about cryptic species within this group. Based on a thorough literature search, we show that the probability of occurrence of cryptic species is mainly related to the number of attempts made to detect them. The use of, both, DNA tools and bioassays significantly increased the probability of cryptic species detection. We did not confirm the generally-accepted idea that species lifestyle (i.e. free-living vs. symbiotic) affects the number of cryptic species. To increase detection of cryptic lineages and to understand the processes leading to cryptic speciation in Acari, integrative approaches including multivariate morphometrics, molecular tools, crossing, ecological assays, intensive sampling, and experimental evolution are recommended. We conclude that there is a demonstrable need for future investigations focusing on potentially hidden mite and tick species and addressing evolutionary mechanisms behind cryptic speciation within Acari. & Anna Skoracka 1 Department of Animal Taxonomy and Ecology, Institute of Environmental Biology, Faculty of Biology, Adam Mickiewicz University, Poznan, Poland 2 Centre for Ecology, Evolution and Environmental Changes (cE3c), Faculty of Science, University of Lisbon, Lisbon, Portugal 3 USDA-ARS, Great Basin Rangelands Research Unit, Reno, NV, USA 4 Department of Avian Biology and Ecology, Institute of Environmental Biology, Faculty of Biology, Adam Mickiewicz University, Poznan, Poland 123 166 Exp Appl Acarol (2015) 67:165–182 Keywords Biodiversity
Cryptic species
Hidden diversity
Integrative approach
Mites and ticks
Molecular systematics
Taxonomy Introduction The evolution of the diversity of life on Earth was called ‘‘the mystery of mysteries’’ by Darwin (1859). The extraordinary diversity of species of mites and ticks (Arachnida: Acari), comprising a vast array of morphological, biological and ecological variation, has inspired acarologists for decades and compels us to understand the evolutionary and ecological processes underlying the origin and proliferation of such diversity. Approximately 55,000 Acari species (including Acariformes and Parasitiformes) have been described, accounting for almost half of all known Arachnida species, and 3.5 % of all Animalia species discovered so far (Zhang 2011). Moreover, estimates of total mite and tick diversity are far greater, reaching 500,000–1,000,000 species (Zhang 2011; Walter and Proctor 2013). One important source of currently hidden Acari diversity is cryptic speciation, i.e. the development of reproductive barriers within an ancestral species that leads to new reproductively isolated species that are virtually identical in their morphology (e.g. Bickford et al. 2007). This poses a challenge to taxonomists, who traditionally distinguish between species based on morphological characters. Such cryptic species are believed to be responsible for gross underestimates of Acari biodiversity. Cryptic species are commonly defined as species that are difficult to distinguish using traditional morphology-based taxonomic methods (Knowlton 1993), or species classified as a single nominal species because they are at least apparently morphologically indistinguishable (Bickford et al. 2007). Some studies explain this phenomenon as a result of recent speciation, after which detectable morphological traits have yet to appear; such cryptic species are evolutionarily young forms that are more similar genetically than more typical, readily distinguishable species (Saez and Lozano 2005; Cooke et al. 2012). There are also empirical examples of cryptic species that do not represent the initial stage of speciation, suggesting the possibility of cryptic speciation in extreme environments or retention of highly conserved morphology due to stabilizing selection in homogenous habitats (Colborn et al. 2001; Lefebure et al. 2006). However, the biological nature of many cryptic species has been questioned by some authors because of the inadequacy of morphological methods or insufficient thoroughness in their application during species description (Knowlton 1993; Lajus et al. 2015). In fact, the application of new technologies (e.g. DNA methods, advanced microscopy) allowed detection of morphological or ecological differences between species previously considered to be cryptic (e.g. Hebert et al. 2004; Padial and de la Riva 2009; Cheng et al. 2011). Regardless of the biological or methodological definition of cryptic species, their presence concerns specialists in a broad range of scientific and applied areas. A thorough understanding of the extent of cryptic diversity within any given taxonomic group is essential not only to assess its overall diversity but also to recognize the complexity of its ecological interactions and evolutionary histories. Given the great economic and medical importance of many mite and tick species, whether as parasites, crop pests, pathogen vectors, or biological control agents (e.g. Navia et al. 2013a; Walter and Proctor 2013), their misidentification may have serious negative consequences for human activities (e.g. Anderson and Trueman 2000; Bernasconi et al. 2002; Arthur et al. 2011; Beati et al. 2013; Matsuda et al. 2013; Miller et al. 2013; Navia et al. 2013b; Skoracka et al. 2013; Burger et al. 2014). Indeed, neglected cryptic diversity may hamper the development of 123 Exp Appl Acarol (2015) 67:165–182 167 technologies and management tools in medicine, agriculture and other important fields, due to the inability to link cryptic species to their unique epidemiological, pathogenic or hostspecific traits (Armstrong and Ball 2005; Pringle et al. 2005; Bickford et al. 2007). Why are cryptic species expected in the Acari? Mites occupy almost every habitat on Earth, with the exception of the water column of the open ocean (Walter and Proctor 2013), but including extreme habitats such as the Antarctic and hypersaline lakes (Stevens and Hogg 2006; Moreno et al. 2008). This ubiquity increases the likelihood that a large number of mite species re (...truncated)