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Finding Evolutionary Processes Hidden in Cryptic Species

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Finding Evolutionary Processes Hidden in Cryptic Species Opinion Finding Evolutionary Processes Hidden in Cryptic Species 1, 2 1,3 1 1 Torsten H. Struck, * Jeffrey L. Feder, Mika Bendiksby, Siri Birkeland, José Cerca, 1 1 1 1,4 Vladimir I. Gusarov, Sonja Kistenich, Karl-Henrik Larsson, Lee Hsiang Liow, 1 1 1 1,5 Michael D. Nowak, Brita Stedje, Lutz Bachmann, and Dimitar Dimitrov Cryptic species could represent a substantial fraction of biodiversity. However, Highlights fi inconsistent definitions and taxonomic treatment of cryptic species prevent Current de nitions of cryptic species are inconsistent and can lead to biased informed estimates of their contribution to biodiversity and impede our under- estimates of species diversity. standing of their evolutionary and ecological significance. We propose a con- Cryptic species are often implied to ceptual framework that recognizes cryptic species based on their low levels of represent taxa displaying low pheno- phenotypic (morphological) disparity relative to their degree of genetic differ- typic disparity in relation to divergence entiation and divergence times as compared with non-cryptic species. We time, but this relationship is usually not formally quantified. discuss how application of a more rigorous definition of cryptic species in taxonomic practice will lead to more accurate estimates of their prevalence in Here we propose a quantitative frame- nature, better understanding of their distribution patterns on the tree of life, and work, which provides a formal charac- terization of the intuitive concept of increased abilities to resolve the processes underlying their evolution. cryptic species. The proposed framework facilitates Cryptic Species – Taxonomic Oddities or Biologically Relevant Entities? understanding of evolutionary pro- ‘ ’ Cryptic species is a common and increasingly used term that refers to taxa that cannot readily cesses leading to and resulting from cryptic species and provides a basis be distinguished morphologically, yet evidence indicates they are on different evolutionary for estimates and modeling of occur- trajectories (Box 1). While researchers may not be able to visually recognize cryptic species as rences of cryptic species across taxa different species, the organisms can. Cryptic species are found on all major branches of the tree and environments. of life and probably represent a significant portion of undiscovered biodiversity [1–4]. As such, The framework fosters a shift from pat- cryptic species might significantly add to our understanding of biodiversity, calling for increased tern- to process-driven research con- conservation efforts [2,4–9]. Cryptic species are also important because they serve as an cerning cryptic species. intellectual bridge connecting the study of taxonomy and phylogenetic pattern with ecosystems functioning, evolutionary processes, and macroevolutionary trends, including speciation, parallelism (see Glossary), convergence, and stasis. However, problems with the definition, ’ among others the linkage to the species taxonomic nomenclature history, and inconsistencies 1 Natural History Museum, University in the use of the term ‘cryptic species’ make it difficult to draw firm conclusions about their of Oslo, 0318 Oslo, Norway 2 prevalence in nature and their implications for ecology and evolution. Department of Biological Sciences, University of Notre Dame, Notre Dame, IN 46556, USA Here, we discuss the general problem of defining cryptic species based on a literature survey 3 NTNU University Museum, that revealed the wide latitude in what researchers call cryptic species. Some authors have Norwegian University of Science and Technology, 7491 Trondheim, Norway even suggested considering cryptic species as a temporary formalization problem of species 4 Centre for Ecological & Evolutionary delineation, rather than as a natural phenomenon [10]. To help mitigate the problem, we Synthesis (CEES), Department of propose a more rigorous, multidimensional, and interdisciplinary approach for cryptic species. Biosciences, University of Oslo, 0316 Oslo, Norway The approach focuses on better quantifying the extent of phenotypic disparity of taxa 5 Current address: Center for compared with the degree to which they have genetically diverged and exchanged genes Macroecology, Evolution and Climate, (have evolved reproductive isolation). Standardizing the delineation of cryptic species will Natural History Museum of Denmark, University of Copenhagen, facilitate investigations into several outstanding questions concerning their biological signifi- Copenhagen, Denmark cance (see Outstanding Questions). It will also lead to a better characterization and Trends in Ecology & Evolution, March 2018, Vol. 33, No. 3 https://doi.org/10.1016/j.tree.2017.11.007 153 © 2017 Elsevier Ltd. All rights reserved. Box 1. Cryptic Species: History and Definitions The English clergyman William Derham reported cryptic species in the avian genus Phylloscopus as early as 1718 [58]. *Correspondence: Cryptic species have thus been recognized for several hundred years. In the last few decades the number of publications [email protected] (T.. Struck). referring tocrypticspecieshasincreaseddramatically (FigureIA), likelyduetomore researchersinthefieldand theincreased use of genetic methods to distinguish taxa (Figure IB and, for example, [5,10]). However, criteria used in the literature to designate taxa as cryptic have often been vague and nonuniform. In the few cases where an explicit definition has been stated, the wording is often similar to that of Bickford et al. [5]: Cryptic species are ‘two or more distinct species that are erroneously classified (and hidden) under one species name’. This taxonomy-based definition is often elaborated upon to highlight that cryptic speciesaremorphologically indistinguishable [5,35]. Others have includedan additionalrequirementof genetic divergence or distinctiveness between cryptic species ([15]; see Supplemental Table S4 online for a list of definitions). How genetically diverged populations must be to be considered cryptic species is usually not specified, but one can assume that this will be of the same magnitude as for non-cryptic species (e.g., a certain barcode gap) [5]. By contrast, several definitions seem to mostly follow trends and concepts related to the research topic of the paper or field of the researcher. For example, in speciation research, definitions tend to highlight reproductive isolation and the biological species concept [37]. Mayr [59], for instance, defined cryptic species as ‘morphologically similar or identical natural populations that are reproductively isolated’. Other terms such as ‘semi-cryptic’, ‘pseudo-cryptic’, ‘sibling’, and ‘hyper- cryptic’ indicating different degrees of ‘crypticity’ have also been proposed [10], complicating the debate of the biological relevance of cryptic species. Regardless, our literature survey (Box 2) revealed that many cryptic species have been defined based on molecular data and taxonomic history, with little regard for actually quantifying morphological disparity. (A) 550 500 450 400 350 300 250 200 # Papers with topic # Papers 150 100 50 1940 1950 1960 1970 1980 1990 2000 2010 2015 Year (B) 70 100 90 60 80 50 70 40 60 50 30 40 Percentage 20 30 20 10 10 # Papers with molecular data 0 0 1978 1980 1985 1990 1995 2000 2005 2010 2015 Year Figure I. Scientific Publications on the Subject of Cryptic Species since 1940. (A) The number of papers found with the search term ‘cryptic speci*’ (dark green line) and ‘cryptic speciation’ (light green). Of note is the marked increase in publications since 1990. (B) The number of papers included in the literature survey (Box 2) that included molecular data in the study (orange line) is also increasing similar to the overall numbers in A. Dark blue bars indicate the percentages of molecular papers that analyzed more than one genetic marker and light blue bars indicate studies based on genomic data. Note that these percentages are not increasing through time. 154 Trends in Ecology & Evolution, March 2018, Vol. 33, No. 3 understanding of the different types of cryptic species, from recently diverged to phylogeneti- Glossary cally distant taxa. In doing so, conclusions concerning (i) evolutionary parallelism, convergence, Convergence: independent and stasis; (ii) the role that cryptic species play in ecosystem functioning; and (iii) factors evolution of a derived character state between taxa from different ancestral initiating and contributing to speciation can be more confidently accepted. traits [41]. Disparity: the morphological or fi The Problem of De nition in Theory and Practice phenotypic difference between taxa Cryptic species have generated both taxonomic and evolutionary ambiguity. A frequently cited [60]. Most recent common ancestor definition of cryptic species [5] describes them as two or more distinct species that were earlier (MRCA): the last ancestor genetically classified as one. Hence, cryptic species are defined based only on their taxonomic nomen- shared by a group of individuals. clature history. However, this is unsatisfactory because various biological factors or taxonomic Parallelism: independent evolution of a character state in different taxa artifacts might result in erroneous species lumping. In addition, it offers no guidance for how from a similar and shared ancestral morphologically similar or by how many characters species should differ to be considered as trait [41]. cryptic. Moreover, one of the longest and most contentious debates in evolution concerns what Pattern-driven research:
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