Molecular Ecology (2014) 23, 4192–4194
NEWS AND VIEWS
PERSPECTIVE
Seeing opportunity in difficulty
Take up the challenge! Opportunities for evolution research from resolving conflict in integrative taxonomy
And ujar et al. (2014) investigated four mitochondrial and three nuclear genes, several morphological traits and the ecological niche from nearly the whole distribution range of the subgenus Mesocarabus (Fig. 1). The interpretation of the outcome was difficult. Winston Churchill once stated ‘a pessimist sees the difficulty in every opportunity; an optimist sees the opportunity in every difficulty’. Here, the authors did see the opportunity in conflict and prioritised certain disciplines over others: For example, they acknowledged that mitochondrial DNA had been introgressed through hybridization and thus does not demarcate species boundaries in this instance (Fig. 2), it still being useful in the heuristic process, though. With their evidence of extensive hybridization and even hybrid speciation, the authors manifest scenarios that were thought very unlikely in animals for long (reviewed by Mallet 2007). As an interesting detail, the authors found pronounced asymmetries among species in the introgression patterns. Finally, with morphological data at hand, the authors also make the link to existing taxonomy and draw nomenclatural consequences, which is both laudable and important (Schlick-Steiner et al. 2007; Carstens et al. 2013). Taxonomic acts are not always possible, for example when the sample is geographically not yet sufficiently comprehensive (Ward & Sumnicht 2012; Arthofer et al. 2013). Often, they have not been published also when possible (reviewed by Schlick-Steiner et al. 2010); only recently, taxonomic acts more often find their way into high-visibility journals (e.g., Satler et al. 2013). Visibility is the cue for a bit of criticism: For maximum accessibility, taxonomic acts should actually be stated
BIRGIT C. SCHLICK-STEINER, WOLFGANG A R T H O F E R and F L O R I A N M . S T E I N E R Molecular Ecology Group, Institute of Ecology, University of Innsbruck, Technikerstr. 25, 6020 Innsbruck, Austria
What’s in a species? The multiple connotations of the question tend to lack simple answers, and not surprisingly so. For example, speciation is a gradual process. Can we say when exactly a child has become an adult? We have precocious youngsters and late bloomers, and often, adults are in some ways childish. There are many triggers for and routes to adolescence. All this holds for speciation, and delimiting species can therefore be a tricky task. Recently, the field of integrative taxonomy has emerged—species delimitation based on multiple sources of evidence. Given that we expect species to exhibit peculiarities in at least one or a few aspects, might it be their alleles of a gene, their morphology, chemistry, behaviour, ecology, reproductive compatibility, or whatever, investigating not just one but several of these aspects makes it more likely that we capture such peculiarities. If the same pattern is found multiply, we talk about agreement among disciplines, and species delimitation is easy. But what if different disciplines tell different stories? Such disagreement makes species delimitation more difficult but is also an opportunity for evolutionary biology (Schlick-Steiner et al. 2010). In this issue of Molecular Ecology, And ujar et al. (2014) present a comprehensive integrative-taxonomic case study of Mesocarabus ground beetles including nomenclatural consequences. They resolve extensive disagreement among disciplines by invoking evolutionary explanations, and the process of conflict resolution thus advances knowledge on species boundaries and evolutionary processes simultaneously. Keywords: disagreement among disciplines, hybrid speciation, hybridization, integrative taxonomy, nomenclatural consequences, species delimitation Received 6 June 2014; revised 15 July 2014; accepted 17 July 2014
Correspondence: Florian M. Steiner, Fax: +43 512 507 51799; E-mail: [email protected]
Fig. 1 Carabus lusitanicus, Sierra de Segura, Albacete, Spain (Photograph by Jes us Arribas Merino). © 2014 John Wiley & Sons Ltd
N E W S A N D V I E W S : P E R S P E C T I V E 4193
(d)
(c)
(e)
(b)
(f)
(g)
(a)
(i)
(h)
Fig. 2 Mitochondrial DNA phylogeny and dorsal habitus of representatives of the subgenus Mesocarabus: (a) Carabus riffensis, Rif Massif, Morocco; (b) Carabus problematicus, Pelhrimov, Czech Republic; (c) Carabus dufourii, Villares, Jaen, Spain; (d) Carabus baguenai, Revolcadores, Murcia, Spain; (e) Carabus breuningi, Cabeza de Manzaneda, Ourense, Spain; (f) Carabus macrocephalus barcelecoanus, Roncesvalles, Navarra, Spain; (g) Carabus lusitanicus, Cantalojas, Guadalajara, Spain; (h) C. lusitanicus, Sierra de Baza, Granada, Spain; (i) C. lusitanicus, Caba~ neros, Toledo, Spain. (All photographs by Jes us Arribas Merino).
in the abstract (if not the title), which the authors, unfortunately, did not do in this instance.
Outlook: the self-reinforcing cycle of integrative taxonomy Integrative taxonomy is in an exploratory stage currently, and refinement of protocols is on top of the agenda. For example, various models and assumptions used in computational analyses could be improved. Further advances will hopefully include new ideas for hypothesis-free analyses. Hypothesis-driven analyses can be problematic, in that potential conflicts among data from different disciplines may remain uncovered—a hypothesis can appear corroborated despite being erroneous as the hypothesis-driven approach neglects all alternatives not hypothesized. For some disciplines, the discovery approach seems difficult to implement at first glance. Only recently, there have been attempts at discovery approaches in morphometrics (Ezard
© 2014 John Wiley & Sons Ltd
et al. 2010; Seifert et al. 2014), which could be followed up, and it would be promising to develop comparable protocols for other data sources such as ecological-niche modelling. Another issue is defining rationales for how to proceed when different, sophisticated analyses of the same data have different outcomes. Currently, agreement among such different analyses of the same data is considered important in distinguishing artefact from real conflict (Steiner et al. 2010; Carstens et al. 2013). However, if disagreement arises in such instances, this could, in fact, represent real conflict all the same. Finally, the most important and most difficult aim, from today’s perspective, will be developing quantitative procedures for comparing statistical support across disciplines (Schlick-Steiner et al. 2010) as these would help removing researcher bias from the integrative-taxonomic process. Whatever new developments the future of integrative taxonomy will bring about, it will, in our mind, stay important to embrace real conflict among disciplines. The more we find out on disagreements caused by evolutionary phenomena, on their frequency of occurrence and on the expectable signatures in the data, the better will we perform in delineating species. At the same time, we will fill evolutionary lacunas. For many phenomena, we still lack causal understanding— think of mutation-rate variation, endosymbiont-triggered host phenotypes, adaptation-caused selective sweeps, morphological stasis and/or convergence, pseudogenes or genome duplications. For all these, we are therefore in need of representative study systems. This brings us back to And ujar et al. (2014). Unravelling the causes for disagreement in their data improved our knowledge on hybridization and, moreover, made available questions for in-depth follow-up research in Mesocarabus: Is there an adaptive value to hybridization? What causes asymmetry among species in introgression? Why are different parts of the genome affected differently by hybridization and what can we learn from this (cf. Vines 2014)? In the coming years, an unprecedented amount of genomic data will accumulate (Andrew et al. 2013). If we are ready for taking up the challenge, comparing these genomic with other data will allow us to discover an unprecedented amount of conflict, waiting for resolution via evolutionary explanations. And all the time, our species delimitations will improve.
Acknowledgements We thank Editor Armando Geraldes and an anonymous referee for constructive input that helped improve the paper. B.C.S.-S. was supported by the Austrian Science Fund, FWF (P23409), W.A. by the science fund of the Autonomous Province of South Tyrol (40.3/22306/ 27.01.2014), F.M.S. by the FWF (P25955).
References Andrew RL, Bernatchez L, Bonin A et al. (2013) A road map for molecular ecology. Molecular Ecology, 22, 2605–2626.
4194 N E W S A N D V I E W S : P E R S P E C T I V E And ujar C, Arribas P, Ruiz C, Serrano J, G omez-Zurita J (2014) Integration of conflict into integrative taxonomy: fitting hybridization in species delimitation of Mesocarabus (Coleoptera: Carabidae). Molecular Ecology, 23, 4344–4361. Arthofer W, Rauch H, Thaler-Knoflach B et al. (2013) How diverse is Mitopus morio? Integrative taxonomy detects cryptic species in a small-scale sample of a widespread harvestman. Molecular Ecology, 22, 3850–3863. Carstens BC, Pelletier TA, Reid NM, Satler JD (2013) How to fail at species delimitation. Molecular Ecology, 22, 4369–4383. Ezard THG, Pearson PN, Purvis A (2010) Algorithmic approaches to aid species’ delimitation in multidimensional morphospace. BMC Evolutionary Biology, 10, 175. Mallet J (2007) Hybrid speciation. Nature, 446, 279–283. Satler JD, Carstens BC, Hedin M (2013) Multilocus species delimitation in a complex of morphologically conserved trapdoor spiders (Mygalomorphae, Antrodiaetidae, Aliatypus). Systematic Biology, 62, 805–823. Schlick-Steiner BC, Seifert B, Stauffer C, Christian E, Crozier RH, Steiner FM (2007) Without morphology, cryptic species stay in taxonomic crypsis following discovery. Trends in Ecology & Evolution, 22, 391–392. Schlick-Steiner BC, Steiner FM, Seifert B, Stauffer C, Christian E, Crozier RH (2010) Integrative taxonomy: a multisource approach
to exploring biodiversity. Annual Review of Entomology, 55, 421– 438. Seifert B, Ritz M, Cs} osz S (2014) Application of Exploratory Data Analyses opens a new perspective in morphology-based alphataxonomy of eusocial organisms. Myrmecological News, 19, 1–15. Steiner FM, Seifert B, Moder K, Schlick-Steiner BC (2010) A multisource solution for a complex problem in biodiversity research: description of the cryptic ant species Tetramorium alpestre sp.n. (Hymenoptera: Formicidae). Zoologischer Anzeiger, 249, 223–254. Vines TH (2014) Stuck in the middle with you: close concordance between geographical clines in a cricket hybrid zone. Molecular Ecology, 23, 1647–1649. Ward PS, Sumnicht TP (2012) Molecular and morphological evidence for three sympatric species of Leptanilla (Hymenoptera: Formicidae) on the Greek island of Rhodes. Myrmecological News, 17, 5–11.
This paper was written by B.C.S.-S., W.A. and F.M.S. doi: 10.1111/mec.12868
© 2014 John Wiley & Sons Ltd
NEWS AND VIEWS
PERSPECTIVE
Seeing opportunity in difficulty
Take up the challenge! Opportunities for evolution research from resolving conflict in integrative taxonomy
And ujar et al. (2014) investigated four mitochondrial and three nuclear genes, several morphological traits and the ecological niche from nearly the whole distribution range of the subgenus Mesocarabus (Fig. 1). The interpretation of the outcome was difficult. Winston Churchill once stated ‘a pessimist sees the difficulty in every opportunity; an optimist sees the opportunity in every difficulty’. Here, the authors did see the opportunity in conflict and prioritised certain disciplines over others: For example, they acknowledged that mitochondrial DNA had been introgressed through hybridization and thus does not demarcate species boundaries in this instance (Fig. 2), it still being useful in the heuristic process, though. With their evidence of extensive hybridization and even hybrid speciation, the authors manifest scenarios that were thought very unlikely in animals for long (reviewed by Mallet 2007). As an interesting detail, the authors found pronounced asymmetries among species in the introgression patterns. Finally, with morphological data at hand, the authors also make the link to existing taxonomy and draw nomenclatural consequences, which is both laudable and important (Schlick-Steiner et al. 2007; Carstens et al. 2013). Taxonomic acts are not always possible, for example when the sample is geographically not yet sufficiently comprehensive (Ward & Sumnicht 2012; Arthofer et al. 2013). Often, they have not been published also when possible (reviewed by Schlick-Steiner et al. 2010); only recently, taxonomic acts more often find their way into high-visibility journals (e.g., Satler et al. 2013). Visibility is the cue for a bit of criticism: For maximum accessibility, taxonomic acts should actually be stated
BIRGIT C. SCHLICK-STEINER, WOLFGANG A R T H O F E R and F L O R I A N M . S T E I N E R Molecular Ecology Group, Institute of Ecology, University of Innsbruck, Technikerstr. 25, 6020 Innsbruck, Austria
What’s in a species? The multiple connotations of the question tend to lack simple answers, and not surprisingly so. For example, speciation is a gradual process. Can we say when exactly a child has become an adult? We have precocious youngsters and late bloomers, and often, adults are in some ways childish. There are many triggers for and routes to adolescence. All this holds for speciation, and delimiting species can therefore be a tricky task. Recently, the field of integrative taxonomy has emerged—species delimitation based on multiple sources of evidence. Given that we expect species to exhibit peculiarities in at least one or a few aspects, might it be their alleles of a gene, their morphology, chemistry, behaviour, ecology, reproductive compatibility, or whatever, investigating not just one but several of these aspects makes it more likely that we capture such peculiarities. If the same pattern is found multiply, we talk about agreement among disciplines, and species delimitation is easy. But what if different disciplines tell different stories? Such disagreement makes species delimitation more difficult but is also an opportunity for evolutionary biology (Schlick-Steiner et al. 2010). In this issue of Molecular Ecology, And ujar et al. (2014) present a comprehensive integrative-taxonomic case study of Mesocarabus ground beetles including nomenclatural consequences. They resolve extensive disagreement among disciplines by invoking evolutionary explanations, and the process of conflict resolution thus advances knowledge on species boundaries and evolutionary processes simultaneously. Keywords: disagreement among disciplines, hybrid speciation, hybridization, integrative taxonomy, nomenclatural consequences, species delimitation Received 6 June 2014; revised 15 July 2014; accepted 17 July 2014
Correspondence: Florian M. Steiner, Fax: +43 512 507 51799; E-mail: [email protected]
Fig. 1 Carabus lusitanicus, Sierra de Segura, Albacete, Spain (Photograph by Jes us Arribas Merino). © 2014 John Wiley & Sons Ltd
N E W S A N D V I E W S : P E R S P E C T I V E 4193
(d)
(c)
(e)
(b)
(f)
(g)
(a)
(i)
(h)
Fig. 2 Mitochondrial DNA phylogeny and dorsal habitus of representatives of the subgenus Mesocarabus: (a) Carabus riffensis, Rif Massif, Morocco; (b) Carabus problematicus, Pelhrimov, Czech Republic; (c) Carabus dufourii, Villares, Jaen, Spain; (d) Carabus baguenai, Revolcadores, Murcia, Spain; (e) Carabus breuningi, Cabeza de Manzaneda, Ourense, Spain; (f) Carabus macrocephalus barcelecoanus, Roncesvalles, Navarra, Spain; (g) Carabus lusitanicus, Cantalojas, Guadalajara, Spain; (h) C. lusitanicus, Sierra de Baza, Granada, Spain; (i) C. lusitanicus, Caba~ neros, Toledo, Spain. (All photographs by Jes us Arribas Merino).
in the abstract (if not the title), which the authors, unfortunately, did not do in this instance.
Outlook: the self-reinforcing cycle of integrative taxonomy Integrative taxonomy is in an exploratory stage currently, and refinement of protocols is on top of the agenda. For example, various models and assumptions used in computational analyses could be improved. Further advances will hopefully include new ideas for hypothesis-free analyses. Hypothesis-driven analyses can be problematic, in that potential conflicts among data from different disciplines may remain uncovered—a hypothesis can appear corroborated despite being erroneous as the hypothesis-driven approach neglects all alternatives not hypothesized. For some disciplines, the discovery approach seems difficult to implement at first glance. Only recently, there have been attempts at discovery approaches in morphometrics (Ezard
© 2014 John Wiley & Sons Ltd
et al. 2010; Seifert et al. 2014), which could be followed up, and it would be promising to develop comparable protocols for other data sources such as ecological-niche modelling. Another issue is defining rationales for how to proceed when different, sophisticated analyses of the same data have different outcomes. Currently, agreement among such different analyses of the same data is considered important in distinguishing artefact from real conflict (Steiner et al. 2010; Carstens et al. 2013). However, if disagreement arises in such instances, this could, in fact, represent real conflict all the same. Finally, the most important and most difficult aim, from today’s perspective, will be developing quantitative procedures for comparing statistical support across disciplines (Schlick-Steiner et al. 2010) as these would help removing researcher bias from the integrative-taxonomic process. Whatever new developments the future of integrative taxonomy will bring about, it will, in our mind, stay important to embrace real conflict among disciplines. The more we find out on disagreements caused by evolutionary phenomena, on their frequency of occurrence and on the expectable signatures in the data, the better will we perform in delineating species. At the same time, we will fill evolutionary lacunas. For many phenomena, we still lack causal understanding— think of mutation-rate variation, endosymbiont-triggered host phenotypes, adaptation-caused selective sweeps, morphological stasis and/or convergence, pseudogenes or genome duplications. For all these, we are therefore in need of representative study systems. This brings us back to And ujar et al. (2014). Unravelling the causes for disagreement in their data improved our knowledge on hybridization and, moreover, made available questions for in-depth follow-up research in Mesocarabus: Is there an adaptive value to hybridization? What causes asymmetry among species in introgression? Why are different parts of the genome affected differently by hybridization and what can we learn from this (cf. Vines 2014)? In the coming years, an unprecedented amount of genomic data will accumulate (Andrew et al. 2013). If we are ready for taking up the challenge, comparing these genomic with other data will allow us to discover an unprecedented amount of conflict, waiting for resolution via evolutionary explanations. And all the time, our species delimitations will improve.
Acknowledgements We thank Editor Armando Geraldes and an anonymous referee for constructive input that helped improve the paper. B.C.S.-S. was supported by the Austrian Science Fund, FWF (P23409), W.A. by the science fund of the Autonomous Province of South Tyrol (40.3/22306/ 27.01.2014), F.M.S. by the FWF (P25955).
References Andrew RL, Bernatchez L, Bonin A et al. (2013) A road map for molecular ecology. Molecular Ecology, 22, 2605–2626.
4194 N E W S A N D V I E W S : P E R S P E C T I V E And ujar C, Arribas P, Ruiz C, Serrano J, G omez-Zurita J (2014) Integration of conflict into integrative taxonomy: fitting hybridization in species delimitation of Mesocarabus (Coleoptera: Carabidae). Molecular Ecology, 23, 4344–4361. Arthofer W, Rauch H, Thaler-Knoflach B et al. (2013) How diverse is Mitopus morio? Integrative taxonomy detects cryptic species in a small-scale sample of a widespread harvestman. Molecular Ecology, 22, 3850–3863. Carstens BC, Pelletier TA, Reid NM, Satler JD (2013) How to fail at species delimitation. Molecular Ecology, 22, 4369–4383. Ezard THG, Pearson PN, Purvis A (2010) Algorithmic approaches to aid species’ delimitation in multidimensional morphospace. BMC Evolutionary Biology, 10, 175. Mallet J (2007) Hybrid speciation. Nature, 446, 279–283. Satler JD, Carstens BC, Hedin M (2013) Multilocus species delimitation in a complex of morphologically conserved trapdoor spiders (Mygalomorphae, Antrodiaetidae, Aliatypus). Systematic Biology, 62, 805–823. Schlick-Steiner BC, Seifert B, Stauffer C, Christian E, Crozier RH, Steiner FM (2007) Without morphology, cryptic species stay in taxonomic crypsis following discovery. Trends in Ecology & Evolution, 22, 391–392. Schlick-Steiner BC, Steiner FM, Seifert B, Stauffer C, Christian E, Crozier RH (2010) Integrative taxonomy: a multisource approach
to exploring biodiversity. Annual Review of Entomology, 55, 421– 438. Seifert B, Ritz M, Cs} osz S (2014) Application of Exploratory Data Analyses opens a new perspective in morphology-based alphataxonomy of eusocial organisms. Myrmecological News, 19, 1–15. Steiner FM, Seifert B, Moder K, Schlick-Steiner BC (2010) A multisource solution for a complex problem in biodiversity research: description of the cryptic ant species Tetramorium alpestre sp.n. (Hymenoptera: Formicidae). Zoologischer Anzeiger, 249, 223–254. Vines TH (2014) Stuck in the middle with you: close concordance between geographical clines in a cricket hybrid zone. Molecular Ecology, 23, 1647–1649. Ward PS, Sumnicht TP (2012) Molecular and morphological evidence for three sympatric species of Leptanilla (Hymenoptera: Formicidae) on the Greek island of Rhodes. Myrmecological News, 17, 5–11.
This paper was written by B.C.S.-S., W.A. and F.M.S. doi: 10.1111/mec.12868
© 2014 John Wiley & Sons Ltd
