Operational criteria for cryptic species delimitation when evidence is limited, as exemplified by North AmericanEntomobrya(Collembola: Entomobryidae)

Abstract

Evaluating species boundaries remains a significant challenge in rare, difficult to collect, and/or understudied groups because of a lack of available data. Uninformative morphology, unknown ecologies and/or geographical distributions, inadequate comparative sequence data, and limited sample sizes present substantial challenges when applying commonly used methods for species delimitation. Here we present an approach that overcomes the challenges previously mentioned by integrating phylogeny, genetic distances, and a fixed diagnostic character (i.e. colour pattern) into the species delimitation process. The genus Entomobrya (Collembola) includes many species marked by complex and variable colour patterns. Many Entomobrya species have been named based exclusively on colour pattern, but the value of this character as a species-level diagnostic marker has been challenged. To test the hypothesis that colour forms in Entomobrya represent independent evolutionary lineages, i.e. distinct species, we used phylogenetic methods to evaluate the association between colour pattern and molecular variation in the cytochrome c oxidase I gene (COI) in 11 species of North American Entomobrya. The comparative analysis focused on 13 colour forms distributed amongst the species Entomobrya assuta, Entomobrya clitellaria, Entomobrya ligata, and Entomobrya quadrilineata. Phylogenetic analysis and genetic divergences sorted the 13 colour forms into seven independent evolutionary lineages, including three morphologically cryptic lineages diagnosable by colour pattern. However, genetic divergence did not always correlate with colour pattern variation, indicating that the diagnostic utility of colour pattern is species dependent and requires individual evaluation for each species. We propose that incorporation of the explicit species delimitation criteria developed for this study will result in a substantial advance in the identification and description of species in understudied taxa.

Taxonomic review and phylogenetic analysis of fifteen North American Entomobrya (Collembola, Entomobryidae), including four new species

“…n. 1 and Entomobrya sp. n. 2 in Katz et al (2015). The cryptic lineages of Entomobrya quadrilineata color forms B, C, and D in Katz et al (2015) are identified as Entomobrya decemfasciata .…”

“…For some groups, however, uncertain homology, intraspecific variation, and characters of difficult observation have limited the utility of morphological characters as tools for species diagnosis and phylogenetic inference. Recent advances in DNA sequencing technology have provided scientists with additional ways to delimit groups that lack informative morphology, such as cryptic species complexes (Frati et al 1994, 1995, 2000; Carapelli et al 1995, 2005; Simonsen et al 1999; Soto-Adames 2002; Burkhardt and Filser 2005; Cicconardi et al 2010, 2013; Felderhoff et al 2010; Porco et al 2012; Zhang et al 2014c; Katz et al 2015), but in practice most species diagnosis remains dependent on fixed characters, only obtained by rigorous morphological examination (Will and Rubinoff 2004). …”

“…Therefore, the primary goal of this study is to examine and document Entomobrya chaetotaxy to provide detailed descriptions and figures in order to clarify species boundaries and to simplify the diagnosis of eastern North American Entomobrya species. A total of 15 species of North American Entomobrya that occur east of the Mississippi River are examined and described with special emphasis on chaetotaxy and color pattern, including three cryptic species lineages identified by Katz et al (2015) and two new species. Additionally, phylogenies, incorporating both the morphology described in this study and molecular COI sequences from Katz et al (2015), are presented in order to explore how chaetotaxy and other morphological characters affect phylogenetic estimation.…”

Groping through the black box of variability: An integrative taxonomic and nomenclatural re-evaluation of Zospeum isselianum Pollonera, 1887 and allied species using new imaging technology (Nano-CT, SEM), conchological, histological and molecular data (Ellobioidea, Carychiidae)

“…are not directly practicable. Morphological stasis or overlapping intra-and interspecific character variability often confuse interpretation of species (hypotheses) and confound conventional species delimitation approaches (de Queiroz 2007, Katz et al 2015. In our case with subterranean ellobioid microsnails, integrative taxonomy provides the most tangible answer to this problem since it pulls together data derived from different data sources including comparative morphology, genetics, ecology and geology to enable inferences about founded, but sketchy species hypotheses.…”

“…In addition, species delimitation, the practice of recognizing and determining species boundaries, has expanded to evaluate the current inflation of species concepts generated to infer biological information (de Queiroz 2000, Katz et al 2015). Speciation is an ongoing process influencing traits at varying temporal scales.…”