Cryptic Species or Inadequate Taxonomy? Implementation of 2D Geometric Morphometrics Based on Integumental Organs as Landmarks for Delimitation and Description of Copepod Taxa

Abstract

Discovery of cryptic species using molecular tools has become common in many animal groups but it is rarely accompanied by morphological revision, creating ongoing problems in taxonomy and conservation. In copepods, cryptic species have been discovered in most groups where fast-evolving molecular markers were employed. In this study at Yeelirrie in Western Australia we investigate a subterranean species complex belonging to the harpacticoid genus Schizopera Sars, 1905, using both the barcoding mitochondrial COI gene and landmark-based two-dimensional geometric morphometrics. Integumental organs (sensilla and pores) are used as landmarks for the first time in any crustacean group. Complete congruence between DNA-based species delimitation and relative position of integumental organs in two independent morphological structures suggests the existence of three distinct evolutionary units. We describe two of them as new species, employing a condensed taxonomic format appropriate for cryptic species. We argue that many supposedly cryptic species might not be cryptic if researchers focus on analyzing morphological structures with multivariate tools that explicitly take into account geometry of the phenotype. A perceived supremacy of molecular methods in detecting cryptic species is in our view a consequence of disparity of investment and unexploited recent advancements in morphometrics among taxonomists. Our study shows that morphometric data alone could be used to find diagnostic morphological traits and gives hope to anyone studying small animals with a hard integument or shell, especially opening the door to assessing fossil diversity and rich museum collections. We expect that simultaneous use of molecular tools with geometry-oriented morphometrics may yield faster formal description of species. Decrypted species in this study are a good example for urgency of formal descriptions, as they display short-range endemism in small groundwater calcrete aquifers in a paleochannel, where their conservation may be threatened by proposed mining.

Two in one: cryptic species discovered in biological control agent populations using molecular data and crossbreeding experiments

“…The use of alternative data sources, such as ISSR, morphology and mating experiments in this study, can act as checks on these possible sources of error (Karanovic et al. ; Dejaco et al. In press), as can more laborious methodological controls, although such practices compromise barcoding's claim to be a fast and efficient method of species discovery and delimitation (Song et al.…”

“…Other problems associated with DNA-barcoding are the presence of mitochondrial DNA sequences in the nuclear genome (numts) and heteroplasmy (more than one mitochondrial genome; Song et al 2008). The use of alternative data sources, such as ISSR, morphology and mating experiments in this study, can act as checks on these possible sources of error (Karanovic et al 2016;Dejaco et al In press), as can more laborious methodological controls, although such practices compromise barcoding's claim to be a fast and efficient method of species discovery and delimitation (Song et al 2008).…”

Cryptic species as a window into the paradigm shift of the species concept

“…Noteworthy, some authors have already coined a term “pseudo‐cryptic” to distinguish “completely identical species” from “morphologically diagnosable species” (Achurra, Rodriguez, & Erséus, ; Knowlton, ; Sáez & Lozano, ). This classification may lead to questions such as “When are species similar enough to be considered morphologically cryptic?” (Karanovic et al., ; Lajus, Sukhikh, & Alekseev, ). This question is at risk to remain without epilogue.…”

“…Many authors stated that perfect morphological similarity does not exist and that morphological analyses based on molecular species delimitation often yield morphological distinctness. Hence, some researchers consider the concept of cryptic species as overrated (Jugovic, Jalžić, Prevorčnik, & Sket, ; Karanovic, Djurakic, & Eberhard, ; Knowlton, ; Zúñiga‐Reinoso & Benítez, ). Noteworthy, some authors have already coined a term “pseudo‐cryptic” to distinguish “completely identical species” from “morphologically diagnosable species” (Achurra, Rodriguez, & Erséus, ; Knowlton, ; Sáez & Lozano, ).…”

Different roads lead to Rome: Integrative taxonomic approaches lead to the discovery of two new lizard lineages in theLiolaemus montanusgroup (Squamata: Liolaemidae)

“…In addition, the General Lineage Concept (de Queiroz, 1998(de Queiroz, , 2007 explicitly recognizes a 'grey zone' or fuzzy boundary where populations in various stages of divergence have not fully completed a speciation process, and under which all methods for delimiting species will occasionally fail or be discordant with each other (Sites & Marshall, 2003. However, an IT approach can provide evolutionary explanations for discordant species criteria and uncover complex evolutionary histories (Dejaco et al, 2016;Karanovic, Djurakic & Eberhard, 2016). Table 3.…”