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First Case of Parthenogenesis in Ladybirds

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First Case of Parthenogenesis in Ladybirds First case of parthenogenesis in ladybirds (Coleoptera: Coccinellidae) suggests new mechanisms for the evolution of asexual reproduction Alexandra Magro, Emilie Lecompte, Jean-Louis Hemptinne, António Soares, Anne-marie Dutrillaux, Jérôme Murienne, Helmut Fürsch, Bernard Dutrillaux To cite this version: Alexandra Magro, Emilie Lecompte, Jean-Louis Hemptinne, António Soares, Anne-marie Dutrillaux, et al.. First case of parthenogenesis in ladybirds (Coleoptera: Coccinellidae) suggests new mecha- nisms for the evolution of asexual reproduction. Journal of Zoological Systematics and Evolutionary Research, Wiley, 2020, 58 (1), pp.194-208. 10.1111/jzs.12339. hal-02404220 HAL Id: hal-02404220 https://hal.archives-ouvertes.fr/hal-02404220 Submitted on 4 Feb 2021 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. Received: 18 January 2019 | Revised: 24 July 2019 | Accepted: 30 July 2019 DOI: 10.1111/jzs.12339 ORIGINAL ARTICLE First case of parthenogenesis in ladybirds (Coleoptera: Coccinellidae) suggests new mechanisms for the evolution of asexual reproduction Alexandra Magro1,2 | Emilie Lecompte1,3 | Jean‐Louis Hemptinne1,2 | Antonio O. Soares4 | Anne‐Marie Dutrillaux5 | Jérôme Murienne1,3 | Helmut Fürsch6 | Bernard Dutrillaux5 1Laboratoire Evolution et Diversité biologique, UMR EDB 5174 CNRS / UT3 / Abstract IRD, Toulouse, France Parthenogenesis, the development of unfertilized eggs resulting in the exclusive pro‐ 2 Ecole Nationale Supérieure de Formation duction of female offspring, is rare in animals relative to sexual reproduction and de l'Enseignement Agricole, Auzeville‐ Tolosane, France is mainly reported in invertebrates. It has been hypothesized that polyploidy, hy‐ 3Université Toulouse III‐Paul Sabatier, bridization and endosymbiont infections are its major causal events but the mecha‐ Toulouse, France nisms triggering asexual reproduction remain unclear. Here, we study the proximate 4Centre for Ecology, Evolution and Environmental Changes, Azorean causes at the origin of parthenogenesis in the first reported case of asexuality in Biodiversity Group, University of the Azores, the Coccinellidae (Coleoptera). The asexual populations were found in the Azores Ponta Delgada, Azores, Portugal and the Mascarene archipelagos, and were identified as Nephus voeltzkowi Weise, a 5Institut de Systématique, Evolution, Biodiversité, UMR ISYEB 7205 CNRS / bisexual species widespread in sub‐Saharan Africa. The specimens from both popu‐ MNHN / UPMC / EPHE, Museum National lations are diploid but present different karyotypes and heterozygosities that evoke d'Histoire Naturelle, Paris, France 6Zoologische Staatssammlung München, hybrid origins, commonly associated with parthenogenesis in Coleoptera. However, Munich, Germany the close proximity of their genomes (99.8% homology for the complete mitochon‐ Correspondence drial genome and 99.9% for the complete nuclear ribosomal cluster) together with the Alexandra Magro, Laboratoire Evolution et congruence between the mtDNA tree and the nuclear tree, and the low heterozygo‐ Diversité biologique, UMR EDB 5174 CNRS/ UT3 / IRD, 118 rt de Narbonne Bt 4R1, sity levels, suggests that the two populations are not hybrid. We propose that they 31062 Toulouse cedex 9, France. belong to a single chromosomally polymorphic species undergoing Robertsonian fu‐ Email: alexandra.magro@univ‐tlse3.fr sions. Furthermore, specimens from both populations are infected with Wolbachia Funding information (supergroup B strain), contrary to sympatric bisexual species of the same genus. “Laboratoire d'Excellence” LabEx TULIP, Grant/Award Number: ANR‐10‐LABX‐41; Although Wolbachia has been shown to induce parthenogenesis in haplodiploid or‐ "Laboratoire d'Excellence" LabEx CEBA, ganisms, it has been recently suggested that it could also induce parthenogenesis in Grant/Award Number: ANR‐10‐LABX‐25‐01 hosts with other sex determination systems. Whether chromosome rearrangements and/or Wolbachia infections are post‐parthenogenetic events or are at the origin of parthenogenesis still needs to be determined. KEYWORDS insularity, Nephus, Robertsonian translocations, the “mate scarcity hypothesis”, Wolbachia Contributing authors: Emilie Lecompte (emilie.lecompte@univ‐tlse3.fr); Jean‐Louis Hemptinne (jean‐louis.hemptinne@univ‐tlse3.fr); Antonio O. Soares ([email protected]); Anne‐Marie Dutrillaux ([email protected]); Jérôme Murienne (jerome.murienne@univ‐tlse3.fr); Helmut Fürsch (coleja@t‐online.de); Bernard Dutrillaux ([email protected]) 194 | © 2019 Blackwell Verlag GmbH wileyonlinelibrary.com/journal/jzs J Zool Syst Evol Res. 2020;58:194–208. MAGRO ET AL. | 195 1 | INTRODUCTION as a consequence of hybridization and/or polyploidy (Bullini, 1994; Kearney, 2005; Lundmark, 2006; Simon et al., 2003). Polyploidy is Asexual reproduction is infrequent in animals, sexual reproduction further subdivided into allopolyploidy and autopolyploidy: in the first being the overwhelming trend. The development of unfertilized eggs case, the chromosomes come from two different species following resulting in the exclusive production of female offspring, usually known hybridization, and, in the second, chromosomes result from the same as parthenogenesis (Simon, Delmotte, Rispe, & Crease, 2003), is mainly genome (Stenberg & Saura, 2009). Finally, some microorganisms, reported in invertebrates (Sinclair, Pramuk, Bezy, Crandall, & Sites, Wolbachia being the most frequent, can manipulate the reproductive 2010). In insects and other Hexapoda, approximately 1,100 species are system of arthropods and induce the appearance of parthenogenesis thought to reproduce by obligate parthenogenesis (i.e., females lay eggs (Werren, Baldo, & Clark, 2008). The precise mechanism at the origin that all develop into females, without any mating at all) (Normark, 2014). of parthenogenesis and the frequency with which asexuality events The prominent hypothesis for the rareness of asexual reproduction occur (the advent in a population of a single clonal line or several is that, although there may be a twofold reproductive advantage in it, lines with different genotypes) lead to different degrees of genetic by sparing male production, asexual lines cumulate deleterious muta‐ variability in asexual populations, with important consequences for tions leading to their long‐term extinction. This said, some asexual lines their evolutionary success. Nevertheless, although there is abundant have been present on Earth for millions of years (Heethoff, Norton, literature on the subject, the mechanisms triggering asexual repro‐ Scheu, & Maraun, 2009; Mark Welch, Ricci, & Meselson, 2009; Schön, duction remain unclear (Bullini, 1994; Choleva et al., 2012; Neiman, Rossetti, & Martens, 2009). Therefore, although uni‐parental forms of Sharbel, & Schwander, 2014). reproduction are generally considered to be disadvantageous, this be‐ The Coccinellidae is a very diversified family composed of some lief should be qualified: every case of asexuality thrives in a particular 6,000 species (Vandenberg, 2002). It has been extensively studied ecological context, and is under unique selective processes (Archetti, from a systematics, ecological and applied (e.g., biological control, in‐ 2010; Bengtsson, 2009). Several theories discuss the conditions that vasion) point of view, both in the field and in the laborator y (see Hodek, would allow asexual lines to maintain themselves, to coexist with their van Emden, & Honěk, 2012 for a comprehensive revision). Skewed sexual counterparts but also to eventually compete and ultimately sex ratios are common in ladybirds and are the result of infections by drive the latter to extinction (Archetti, 2010; Engelstädter, 2017; endosymbionts acting as male killers (Weinert, Tinsley, Temperley, & Rice & Friberg, 2009). The circumstances and mechanisms underly‐ Jiggins, 2007) but so far, parthenogenesis has never been mentioned ing parthenogenesis but also studies of niche breadth, life histories, for the family. However, during fieldwork in two distantly located bio‐ competition, predation and parasitism are essential to understanding diversity hot spots, Santa Maria Island—Azores archipelago (Atlantic the evolutionary history of asexual populations. In this study, we are Ocean, Northern hemisphere) and Reunion Island—Mascarene archi‐ interested in the proximate causes at the origin of parthenogenesis. pelago (Indian Ocean, Southern hemisphere), we found only females Generally, parthenogenesis is considered as developing spon‐ of Nephus voeltzkowi Weise (Weise, 1910), which raises the question taneously as a result of a mutation within the sexual population or of the possible existence of parthenogenesis in the family. FIGURE 1 Range distribution of Nephus voeltzkowi Weise and collection sites (Azores archipelago; Reunion island) of the all‐female populations 196 | MAGRO ET AL. Nephus voeltzkowi belongs to the Scymninae subfamily and is a tray to inspect trees and bushes, and a sweeping net for lower coccid, particularly mealybug (Homoptera: Pseudococcidae) pred‐ vegetation.
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