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Publications Files/2011 Dapporto Et Al Pyronia.Pdf Journal of Biogeography (J. Biogeogr.) (2011) 38, 854–867 ORIGINAL Phylogenetic island disequilibrium: ARTICLE evidence for ongoing long-term population dynamics in two Mediterranean butterflies Leonardo Dapporto1*, Thomas Schmitt2, Roger Vila3, Stefano Scalercio4, Heinrich Biermann5, Vlad Dinca˘6,7, Severiano F. Gayubo8, Jose´ A. Gonza´lez8, Pietro Lo Cascio9 and Roger L. H. Dennis10,11 1Istituto Comprensivo Materna Elementere ABSTRACT Media Convenevole da Prato via 1° Maggio 40, Aim Our aims were to verify the existence of phylogenetic disequilibrium 59100 Prato, Italy, 2Department of Biogeography, Trier University, D-54296 Trier, between butterfly lineages at the subcontinental scale for islands and the nearest Germany, 3ICREA and Institute of mainland and to test the capacity of islands for hosting ancestral populations of Evolutionary Biology (CSIC-UPF), Passeig butterflies and the significance of such relict populations. Marı´tim de la Barceloneta 37-49, 08003 Location The western Mediterranean continental area of Europe and North 4 Barcelona, Spain, CRA Centro di Ricerca per Africa together with several large and small islands (Balearics, Tuscan l’Olivicoltura e l’Industria Olearia, I-87036 Archipelago, Aeolian Archipelago, Capri, Sardinia, Sicily, Corsica). Rende (Cosenza), Italy, 5Markusstrasse 17, D-3490, Bad Driburg, Germany, 6Institute of Methods Using geometric morphometrics, the shape of male genitalia was Evolutionary Biology (CSIC-UPF), Passeig analysed in two common butterflies (Pyronia cecilia and Pyronia tithonus), whose Marı´tim de la Barceloneta 37-49, 08003 spatial heterogeneity in the Mediterranean region has recently been described. Barcelona, Spain, 7Departament de Gene`tica i Observed patterns in genital shapes were compared with shapes predicted for Microbiologia, Universitat Auto`noma de islands and fossil islands to assess the contribution of historical and current events Barcelona, 08193 Bellaterra (Barcelona), in accounting for the transition from a refugial model to an equilibrium model. 8 Spain, A´rea de Zoologı´a, Facultad de Biologı´a, Measurements were taken for 473 specimens in 90 insular and mainland sites. Campus ‘Miguel de Unamuno’ Universidad de Salamanca, 37007 Salamanca, Spain, Results The shape of the genitalia of populations of most islands differed 9NESOS, Associazione pro Isole, Corso Vittorio substantially from that predicted by the equilibrium hypothesis while closely Emanuele, 24 98055 Lipari (ME), Italy, fitting the refugial hypothesis. The comparison between different models strongly 10School of Life Sciences, Oxford Brookes suggests that islands maintain ancestral lineages similar to those living in Spain University, Headington, Oxford OX3 0BP, UK, (P. cecilia) and France (P. tithonus). A high correlation between observed and 11Institute for Environment, Sustainability and predicted patterns on islands and fossil islands occurs during the first steps of Regeneration, Mellor Building, Staffordshire modelled introgressive hybridization while the following steps exposed a University, Stoke-on-Trent ST4 2DE, UK successively lower fit, suggesting that the process from a refugial to an equilibrium situation is highly skewed towards an earlier non-equilibrium. Main conclusions The observed non-equilibrium pattern supports the refugial hypothesis, suggesting that an ancestral lineage was originally distributed from Spain to Italy, and also occupied offshore islands. This lineage, replaced in Italy, has persisted on the islands owing to their isolation. A comparison of the distribution patterns for genetic and morphometric markers in several species indicates that the situation highlighted for Pyronia may represent a common *Correspondence: Leonardo Dapporto, Istituto biogeographic feature for many Mediterranean butterflies. Comprensivo Materna Elementere Media Keywords Convenevole da Prato via 1° Maggio 40, 59100, Prato, Italy. Genitalia, geometric morphometrics, glaciations, hybridization, introgression, E-mail: [email protected] Pyronia, refugia, Rhopalocera, western Mediterranean. 854 http://wileyonlinelibrary.com/journal/jbi ª 2011 Blackwell Publishing Ltd doi:10.1111/j.1365-2699.2010.02452.x Phylogenetic disequilibrium in Mediterranean butterflies Furthermore, it is well known that genital shape in Satyrinae INTRODUCTION is very highly correlated with genetic characteristics (e.g. MacArthur & Wilson’s (1967) equilibrium theory of island Cesaroni et al., 1994; Dapporto, 2010a, and literature therein) biogeography represents a milestone in understanding distri- and is perhaps also involved in female choice (Gilligan & bution patterns of species. Despite various criticisms, additions Wenzel, 2008). Consequently, there is strong evidence for the and revisions to their work, the central idea of island existence of many different lineages on islands compared with communities being shaped by complex dynamic interactions those occurring at their nearest mainland sources (Dapporto involving immigration, extinction and evolution is still the et al., 2009; Dapporto, 2010a), as has been demonstrated by basic paradigm of recent island biogeography (Losos & genetic studies (Thomson, 1987; Cesaroni et al., 1994). Ricklefs, 2010). Although most of the work confirming the MacArthur & Wilson (1967) applied their equilibrium equilibrium theory has focused on small and close-to-source theory to species numbers. Subsequently, several authors have islands (e.g. Diamond, 1969; Simberloff & Wilson, 1969; see indicated that processes driving island species richness may also Schoener, 2010, for a recent review), the main advances to also drive changes in the genotypic diversity of their popula- the MacArthur & Wilson model have been formulated with tions (reviewed by Vellend & Orrock, 2010). Mainland–island respect to oceanic islands. On oceanic islands, evolution, and systems that fail to fit equilibrium notions, maintained by consequently speciation, are expected to be more important immigration and extinction, are frequently observed; ‘island than immigration in generating community species diversity disequilibrium’ occurs. Disequilibria are mainly expected to (e.g. Emerson & Gillespie, 2008; Whittaker et al., 2008; Grant arise following natural and anthropogenic disturbance (e.g. & Grant, 2010). On islands located within the range of Bush & Whittaker, 1991; Schoener, 2010) and, interestingly, dispersal capabilities of most taxa, populations are usually disturbance and other changes creating mainland–island assumed to be similar to those on the neighbouring mainland; disequilibria are generally postulated to occur on islands. This ongoing immigration and gene flow is expected to prevent is primarily because mainland areas are assumed to be more island–mainland differentiation. This outcome should be more stable and thus more conservative than island communities evident for taxa with a high dispersal capability (Emerson & (see Fig. 1 of Emerson & Gillespie, 2008, p. 620). Even so, Gillespie, 2008; Lomolino et al., 2010). refugial islands are well known and house exceptional Accordingly, when analysed at the community level, the palaeoendemics [e.g. Lemuriformes on Madagascar (Karanth distributions of flying insects on Mediterranean and European et al., 2005) or Sphenodontia on islands off New Zealand offshore islands (none of which are oceanic) are demonstrated (Jones et al., 2009)]. In addition to such impressive examples, to be closely related to source populations (Dennis & Shreeve, many less prominent, but highly conservative, patterns have 1996; Dennis et al., 2000; Dapporto & Dennis, 2008, 2009; also been demonstrated to occur on Mediterranean islands (see Fattorini, 2009; Heiser & Schmitt, 2010). However, when the Me´dail & Diadema, 2009, for a recent review on plants; and distributions of individual species and infra-specific lineages Sto¨ck et al., 2008, for amphibians). It is also well known that are analysed, their patterns cannot always be explained by species richness, composition and species ranges on mainland means of recent dispersal events (Dapporto & Dennis, 2009, areas can change very rapidly (even over a few decades), 2010; Dapporto et al., 2009; Fattorini, 2009). For instance, on especially in response to human global influences (Fisher et al., west Mediterranean islands, all hitherto analysed Satyrinae 2010); thus, retrodiction of past climatic niche distribution is butterfly species have differently shaped genitalia from those an emerging challenge for macroecology (Nogue´s-Bravo, 2009; occurring on the nearest mainland (Dapporto, 2010a). Habel et al., 2010). Figure 1 Map of the study area: 1, North Africa; 2, Spain; 3, France; 4, northern Italy; 5, southern Italy; 6, Corsica; 7, Sardinia; 8, Sicily; 9, Pianosa; 10, Giglio; 11, Capraia; 12; Elba; 13, Capri; 14, Lipari; 15, Mallorca; 16, Menorca; 17, Piombino; 18, M. Argentario, 19, Montenero; 20, M. Calvi. Journal of Biogeography 38, 854–867 855 ª 2011 Blackwell Publishing Ltd L. Dapporto et al. Butterfly species on Mediterranean islands could well be in possibilities explored ranged from the hypothesis that island disequilibrium with respect to the distribution of mainland populations were maintained for longer or shorter periods as lineages following rapid post-glacial climate changes respon- relicts from any neighbouring mainland influences (refugial sible for shaping most of the genetic structures in this region hypothesis), to the hypothesis that islands no longer host relict (Hewitt, 2001; Schmitt, 2007), especially in view of the rapidity
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