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Integrative Analyses on Western Palearctic Lasiommata Reveal a Mosaic of Nascent Butterfly Species

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Integrative Analyses on Western Palearctic Lasiommata Reveal a Mosaic of Nascent Butterfly Species Received: 13 April 2019 | Revised: 9 October 2019 | Accepted: 22 October 2019 DOI: 10.1111/jzs.12356 ORIGINAL ARTICLE Integrative analyses on Western Palearctic Lasiommata reveal a mosaic of nascent butterfly species Leonardo Platania1 | Raluca Vodă2 | Vlad Dincă3 | Gerard Talavera1 | Roger Vila1 | Leonardo Dapporto4 1Institut de Biologia Evolutiva (CSIC- Universitat Pompeu Fabra), Barcelona, Spain Abstract 2Department of Life Sciences and Systems Satyrinae butterflies occurring in the Mediterranean apparently have reduced gene Biology, University of Turin, Turin, Italy flow over sea straits, and for several species, recent wide-scale biodiversity sur- 3Ecology and Genetics Research Unit, University of Oulu, Oulu, Finland veys indicate the existence of divergent mitochondrial lineages. Here, we apply an 4Dipartimento di Biologia dell'Università di integrative approach and examine the phylogeography of the genus Lasiommata in Firenze, Firenze, Italy the Western Palearctic. Our research comprised molecular analyses (mitochondrial Correspondence and nuclear DNA) and geometric morphometrics (wings and genitalia) for two main Leonardo Platania, Institut de Biologia species groups, and a comparative GMYC analysis, based on COI, of all the tribes Evolutiva (CSIC-Universitat Pompeu Fabra), Barcelona, Spain. within Satyrinae from this region. The GMYC approach revealed a particularly fast Email: [email protected] coalescence rate in the Parargina subtribe. The Lasiommata group was divided into Funding information 12 evolutionary significant units: six clades for the L. maera species group, five for Ministerio de Economía y Competitividad, the L. megera species group, and one for L. petropolitana, with divergences of about Grant/Award Number: CGL2013-48277-P and CGL2016-76322-; Università degli Studi 1%. The patterns of COI were mirrored by ITS2 in L. maera, but the two markers di Firenze; H2020 Marie Skłodowska-Curie were generally inconsistent in L. megera. On the contrary, morphological differences Actions, Grant/Award Number: 609402- 2020 and 625997 were coherent with the results of COI for L. megera, but less clearly so for L. maera. L. paramegaera and L. meadewaldoi were considerably differentiated for all the ana- lyzed markers and likely proceeded faster in the process of speciation because of geographic isolation and reduced effective population size, rendering the rest para- phyletic. Our study illustrates the continuous nature of speciation and the difficulties of delimiting species. In Lasiommata, the recognition of taxa as diverging lineages or distinct, possibly paraphyletic species, mostly depends on the criteria adopted by different species concepts. KEYWORDS COI, ITS2, Lasiommata, morphometrics, speciation 1 | INTRODUCTION become an urgent task in order to better preserve it (Dirzo et al., 2014; Wheeler et al., 2012). Speciation processes manifest as a con- Given alarming rates of biodiversity loss during the Anthropocene, tinuum of divergence, during which recognizing boundaries between understanding how diversity is generated and maintained has species or among populations diverging at various grades may be a difficult matter (Hendry, 2009; Hendry, Bolnick, Berner, & Peichel, Contributing authors: Raluca Vodă ([email protected]), Vlad Dincă (vlad.e.dinca@ 2009; Mallet, Beltrán, Neukirchen, & Linares, 2007; Nosil, Harmon, gmail.com), Gerard Talavera ([email protected]), Roger Vila ([email protected]), Leonardo Dapporto ([email protected]). & Seehausen, 2009; Seehausen, 2009; Shaw & Mullen, 2014). J Zool Syst Evol Res. 2020;00:1–14. wileyonlinelibrary.com/journal/jzs © 2020 Blackwell Verlag GmbH | 1 2 | PLATANIA ET al. This is attested by the existence of a high number of species con- mitochondrial lineages within generally accepted species, suggest- cepts, which sometimes disagree in recognizing if particular taxa ing ongoing differentiation or even the presence of cryptic species should be considered as distinct species (de Queiroz, 2005, 2007). (Dincă, Dapporto, & Vila, 2011; Dincă, Lukhtanov, & Talavera, 2011; In the speciation continuum, a large number of genes, expressing Dincă et al., 2015; Dincă, Zakharov, Hebert, & Vila, 2011; Hausmann a wide array of functional/phenotypic traits, are expected to diverge et al., 2011). Some of these cases have been subsequently studied at varied rates, producing discrepancies of traits between popula- in more detail by using integrative approaches and occasionally re- tions (Hendry, 2009; Hendry et al., 2009). According to observed vealed that species diversity is higher than expected even in inten- geographic patterns, speciation events have been traditionally cat- sively studied areas such as Europe (Dapporto, Vodă, Dincă, & Vila, egorized as sympatric, allopatric or parapatric (Butlin, Galindo, & 2014; Dincă, Zakharov, et al., 2011; Habel et al., 2017; Hernández- Grahame, 2008; Coyne & Orr, 2004; Gavrilets, Li, & Vose, 2000; Roldán et al., 2016). Mayr, 1963; Via, 2001). Sympatric speciation is characterized by the In this paper, we analyze the Western Palearctic taxa of the absence of a physical separation between emerging taxa, which di- genus Lasiommata Westwood, 1841, belonging to the Parargina versify uniquely as a consequence of genetic changes affecting eco- subtribe, for which recent wide-scale biodiversity surveys indicate logical and behavioral adaptations (Barluenga, Stölting, Salzburger, the existence of several divergent mitochondrial lineages in the Muschick, & Meyer, 2006; Via, 2001). Allopatric speciation, consid- Mediterranean area (Dapporto et al., 2017; Dincă et al., 2015; Vodă ered as the main mechanism generating biodiversity, occurs in virtu- et al., 2016; Weingartner, Wahlberg, & Nylin, 2006). We hypothe- ally complete geographic separation between populations because sized that (a) the Lasiommata genus, and the Parargina subtribe in physical barriers produced by geological or climatic transformations general, have shorter coalescence rates compared with other sub- or after events of exceptional dispersal and colonization of remote tribes within the Satyrinae occurring in the Palearctic region. To test areas (Coyne & Orr, 2004; Hewitt, 1996, 2000, 2004; Mittelbach & for this hypothesis, we compared the results of a series of GMYC Schemske, 2015). Following allopatric speciation, sister species may analyses among Satyrinae subtribes based on COI data; (b) the main disperse and get into secondary contact (Pigot & Tobias, 2014), but lineages within this species group are likely in an advanced stage full secondary sympatry is frequently delayed due to density-de- of an unusually fast speciation process. To test for this hypothesis pendent phenomena or competition for resources (Waters, 2011; and clarify the systematic relationships within these taxa, we applied Waters, Fraser, & Hewitt, 2013). As a result, most sister, cryptic and an integrative approach, using molecular and morphological traits. sibling species have relatively narrow contact zones (Hewitt, 2004; We sequenced mitochondrial (cytochrome c oxidase subunit I—COI) Waters, 2011; Waters et al., 2013) even in the case of highly mobile and nuclear DNA (internal transcribed spacer 2—ITS2) and analyzed organisms such as butterflies (Vodă, Dapporto, Dincă, & Vila, 2015a, phenotypic markers consisting of wing shape (presumably evolv- 2015b). Secondary contacts can also occur before the speciation ing under strong environmental selection) and genitalia structures process is completed, but the genetic lineages still tend to have very (mostly evolving under sexual selection) (Habel et al., 2017; Hebert, narrow boundaries (Waters, 2011; Waters et al., 2013). In these Cywinska, & Ball, 2003; Hernández-Roldán et al., 2016; Nazari, cases, either lineage fusion or parapatric speciation can eventually Hagen, & Bozano, 2010; Zinetti et al., 2013). take place (Gavrilets et al., 2000). The analysis of genetic and phenotypic traits diverging among populations represents a fundamental resource to understand the 2 | MATERIAL & METHODS speciation process and the mechanisms underlying it. In addition, the results need to be translated into taxonomic hypotheses in 2.1 | Studied species order to categorize biodiversity, a necessity for many applications. Integrative taxonomy, the classification of organisms by integrating In Europe and North Africa, the butterfly genus Lasiommata is rep- information from different features such as morphology, behavior, resented by five generally recognized species: Lasiommata megera cytology, DNA sequences, or ecology, allows a deeper view of the (Linnaeus, 1767), Lasiommata maera (Linnaeus, 1758), Lasiommata visible and hidden layers of diversity, providing researchers the petropolitana (Fabricius, 1787), Lasiommata paramegaera (Hübner, means to explore and investigate groups that were difficult to study [1824]), and Lasiommata meadewaldoi (Rothschild, 1917), although with classical taxonomy and to refine strategies for species delimi- the taxonomic status of the latter two is still debated. The wall brown tation (Padial, Miralles, De la Riva, & Vences, 2010; Schlick-Steiner L. megera is distributed from North Africa, across a large part of Europe et al., 2010). to Western Asia. The northern European border of its range passes Butterflies (Lepidoptera: Papilionoidea) represent one of the through Ireland, Scotland, southern Scandinavia, and the Baltic coun- best-known groups of invertebrates and are well studied in terms of tries. In the Mediterranean basin, it
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