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Biol Invasions (2020) 22:2049–2062 https://doi.org/10.1007/s10530-020-02238-0 (0123456789().,-volV)( 0123456789().,-volV) ORIGINAL PAPER Factors determining variation in colour morph frequencies in invasive Harmonia axyridis populations Alois Honek . Peter M. J. Brown . Zdenka Martinkova . Jiri Skuhrovec . Marek Brabec . Giovanni Burgio . Edward W. Evans . Marc Fournier . Audrey A. Grez . Jan Kulfan . Francesco Lami . Eric Lucas . Bele´n Lumbierres . Antonio Masetti . Timofej Mogilevich . Marina Orlova-Bienkowskaja . William M. Phillips . Xavier Pons . Jan Strobach . Sandra Viglasova . Peter Zach . Tania Zaviezo Received: 21 May 2019 / Accepted: 27 February 2020 / Published online: 13 March 2020 Ó Springer Nature Switzerland AG 2020 Abstract The Harlequin ladybird Harmonia axyr- and time. In contrast, colour polymorphism in invaded idis Pallas, native to eastern Asia, is an invasive, non- regions has been little studied. We examine and try to native species that has recently achieved an almost account for the morph frequencies observed across the worldwide distribution. A conspicuous feature of this different invaded regions. In America, monomorphic species is colour polymorphism of the elytra. In its populations consist of the non-melanic morphs while native area, the populations consist of a recessive non- European populations contain also melanic morphs. In melanic morph, several dominant melanic morphs and particular geographic areas of Europe, the average small numbers of other (rare) morphs. The morph percentage of the non-melanic morphs varied between proportions in native populations have been inten- 78 and 99%. It was highest in the lowlands of northern sively studied and vary with geographic area, climate Italy and central and northern Europe and decreased in the Alps and western (Spain, UK) and eastern (southeast Russia) margins of the recently invaded Electronic supplementary material The online version of this article (https://doi.org/10.1007/s10530-020-02238-0) con- area. In central Europe the frequency of the non- tains supplementary material, which is available to authorized melanic morphs decreased over the course of the year users. A. Honek Á Z. Martinkova Á J. Skuhrovec (&) Á M. Brabec J. Strobach Department of Statistical Modeling, Institute of Computer Crop Research Institute, Drnovska 507, 16106 Prague 6, Sciences ASCR, Prague, Czech Republic Czech Republic e-mail: [email protected] e-mail: [email protected] G. Burgio Á A. Masetti A. Honek Department of Agricultural and Food Science, University e-mail: [email protected] of Bologna, Viale G. Fanin 42, 40127 Bologna, Italy Z. Martinkova e-mail: [email protected] e-mail: [email protected] A. Masetti J. Strobach e-mail: [email protected] e-mail: [email protected] E. W. Evans P. M. J. Brown Department of Biology, Utah State University, Logan, Applied Ecology Research Group, School of Life UT 84322-5305, USA Sciences, Anglia Ruskin University, East Road, e-mail: [email protected] Cambridge CB1 1PT, UK e-mail: [email protected] 123 2050 A. Honek et al. but increased over the years from 2010 to 2018. The H. axyridis in intensive agriculture areas outside of its local differences might thus arise through gradual native range. Several early introduction attempts of H. change of the morph composition of the founder axyridis in Europe (Kuznetsov 1987; Coutanceau invasive, non-native population. However, the varia- 2006) and North America (McClure 1987) were tion in non-melanic morph frequency was not corre- unsuccessful. In contrast, later unintended introduc- lated with climatic characteristics that might affect tions resulted in the spread of the species in North coccinellid polymorphism. The observed rate of America from the late 1980s (Chapin and Brou 1991; change in morph proportions in our data was too Tedders and Schaefer 1994; LaMana and Miller 1996) small to explain the diversification of what was and subsequently in South America (Martins et al. supposedly a uniform invasive, non-native population 2009; Grez et al. 2010), Europe (Adriaens et al. 2003; at the point of introduction. Cuppen et al. 2004; Brown et al. 2008), Africa (Stals 2010; Nedveˇd and Ha´va 2016), western Asia (Biran- Keywords Polymorphism Á Alien species Á vand et al. 2019) and New Zealand (https://www.mpi. Distribution Á Variation Á Climate Á Selection govt.nz/document-vault/12261). Thus, H. axyridis has now spread to all continents except Antarctica (Ca- macho-Cervantes et al. 2017). The invasion into Eur- ope was evidently derived from biological control Introduction introductions mixing with an invasive population from eastern North America (Lombaert et al. 2010). The Harlequin ladybird Harmonia axyridis Pallas In recently colonized areas, H. axyridis is regarded (Coleoptera: Coccinellidae) is native to the east as an efficient aphid natural enemy (Riddick 2017), Palearctic and Oriental regions (Kovar 2007; Orlova- but also an unwelcome competitor and predator of Bienkowskaja et al. 2015). Its recent spread into other members of the aphidophagous guild (Brown several continents where it is non-native has been well et al. 2015; Kenis et al. 2017; Masetti et al. 2018; studied (Roy et al. 2016). In its native range, H. Zaviezo et al. 2019). The abundance and distribution axyridis is an abundant and efficient predator of aphids of H. axyridis has increased dramatically whilst the (Kuznetsov 1975). Due to its qualities as a biological numbers of several native species have decreased, control agent, many attempts were made to introduce M. Fournier Á E. Lucas F. Lami De´partement des Sciences biologiques, Universite´ du Department of Agricultural, Food, Environmental and Que´bec a` Montre´al, CP 8888, Succ. Centre-ville, Animal Sciences, University of Udine, Via delle Scienze Montreal, QC H3C 3P8, Canada 206, 33100 Udine, UD, Italy e-mail: [email protected] e-mail: [email protected] E. Lucas e-mail: [email protected] B. Lumbierres Á X. Pons Department of Crop and Forest Sciences – Agrotecnio A. A. Grez Centre, University of Lleida, Av. Rovira Roure 191, Facultad de Ciencias Veterinarias y Pecuarias, 25198 Lleida, Spain Universidad de Chile, Santiago, Chile e-mail: [email protected] e-mail: [email protected] X. Pons e-mail: [email protected] J. Kulfan Á S. Viglasova Á P. Zach Institute of Forest Ecology, Slovak Academy of Sciences, T. Mogilevich Á M. Orlova-Bienkowskaja Zvolen, Slovakia A.N. Severtsov Institute of Ecology and Evolution, e-mail: [email protected] Russian Academy of Sciences, 33 Leninskiy Prospect, S. Viglasova Moscow, Russia 119071 e-mail: [email protected] e-mail: [email protected] P. Zach M. Orlova-Bienkowskaja e-mail: [email protected] e-mail: [email protected] 123 Factors determining variation in colour morph frequencies 2051 with H. axyridis implicated in the declines. This has conspicua [ spectabilis [ axyridis [ succinea (Tan helped increase interest in this species, with more than and Li 1934; Tan 1946). In the native (and to an extent, 1300 references since 1990 published on Web of introduced) ranges, there are a number of other morphs Science concerning the life cycle, predation beha- found in low proportions, the genetics of which have viour, distribution, and other elements of the ecology not been well studied (e.g. Hosino 1940; Komai 1956; and genetics of H. axyridis (Roy et al. 2016). for a review see Sloggett and Honek 2012). Morph Among the most intensively studied aspects of H. identity is determined by genetic factors. Specifically axyridis biology is its conspicuous colour polymor- the morph is determined by mosaic dominance, which phism, and the genetics, distribution, ecological and itself is shaped by both the dominance relationships evolutionary factors influencing it. Interest in this between colour morph alleles and the expression of a issue has a long history. Patterns of variation of H. transcription factor (pannier); this determines the axyridis, its genetic determination and factors that formation of melanic elements on the elytra (Gautier determine morph distribution have been studied since et al. 2018). A large inversion in the cis-regulatory the 1920s (Dobzhansky 1924; Komai 1956; Timofe- regions of this transcription factor exists between eff-Ressovsky and Svirezhev 1967; Komai and Chino colour morphsand is thought to underly the mainte- 1969) and continue today (Seo et al. 2007; Wang et al. nance of so much variation within populations (Gau- 2009, 2011). tier et al. 2018). An additional factor of phenotypic In its native area the species has over 200 described variation within a morph is temperature during pre- colour morphs, grouped into 15 classes (Tan and Li imaginal development, which modifies the degree of 1934; Hosino 1940; Tan 1946). The individuals are melanisation. In the non-melanic morphs low temper- classified according to the colour pattern of their ature increases the size and number of black spots, elytra. Four major morph groups, light-coloured non- while its effect on the size of red spots in melanic melanic succinea and dark-coloured melanic axyridis, morphs is below the limit of resolution (Michie et al. spectabilis and conspicua (Fig. 1) are among the most 2010). frequent in the species’ native area, where there is The morph frequencies in the native area of H. extensive variation in morph proportions among local axyridis differ among three geographic regions: the populations (Gautier et al. 2018). Succinea morphs insular region (Japan) is characterized by a mixture of have elytra with yellow to red ground colour and on non-melanic and melanic morphs (Komai et al. 1950; each elytron up to nine black spots organised in four Komai 1956; Noriyuki and Osawa 2015), the east transversal rows. Pale coloration of the dorsal side continental region (China, Korea and the Russian Far leads these morphs to be referred to as the ‘‘non- East) is characterized by a high frequency of the non- melanic morphs’’. The ground colour of the three other melanic morphs, while the central Siberian region is morphs mentioned is black.

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