LETTER doi:10.1002/evl3.30 Evolution and comparative ecology of parthenogenesis in haplodiploid arthropods Casper J. van der Kooi,1,2 Cyril Matthey-Doret,1 and Tanja Schwander1 1Department of Ecology and Evolution, University of Lausanne, Lausanne, Switzerland 2E-mail: [email protected] Received June 5, 2017 Accepted September 13, 2017 Changes from sexual reproduction to female-producing parthenogenesis (thelytoky) have great evolutionary and ecological con- sequences, but how many times parthenogenesis evolved in different animal taxa is unknown. We present the first exhaustive database covering 765 cases of parthenogenesis in haplodiploid (arrhenotokous) arthropods, and estimate frequencies of partheno- genesis in different taxonomic groups. We show that the frequency of parthenogenetic lineages extensively varies among groups (0–38% among genera), that many species have both sexual and parthenogenetic lineages and that polyploidy is very rare. Parthenogens are characterized by broad ecological niches: parasitoid and phytophagous parthenogenetic species consistently use more host species, and have larger, polewards extended geographic distributions than their sexual relatives. These differences did not solely evolve after the transition to parthenogenesis. Extant parthenogens often derive from sexual ancestors with rel- atively broad ecological niches and distributions. As these ecological attributes are associated with large population sizes, our results strongly suggests that transitions to parthenogenesis are more frequent in large sexual populations and/or that the risk of extinction of parthenogens with large population sizes is reduced. The species database presented here provides insights into the maintenance of sex and parthenogenesis in natural populations that are not taxon specific and opens perspectives for future comparative studies. KEY WORDS: asexual reproduction, haplodiploidy, Hymenoptera, niche breadth, thelytoky, Thysanoptera, arrhenotoky, poly- ploidy. Impact Summary sis in 765 species in many phylogenetically unrelated groups with vastly different ecologies. The frequency of partheno- The animal kingdom exhibits a great diversity in reproductive genesis greatly varies among groups, and many species com- modes. In addition to the well-known and widespread sexual prise both sexual and parthenogenetic populations. Overall, reproduction, species can reproduce asexually, via partheno- the frequency ranges from 0–1.5% between orders, but in genesis. Males are absent in parthenogenetic species or pop- species-rich genera, parthenogenesis occurs in up to as much ulations. How this diversity in reproductive systems can be as 38% of the species. Polyploidy is very rare (at most 4%), and maintained remains a major question in evolutionary biology. endosymbiont-induced parthenogenesis is suggested to occur We assembled a database of parthenogenetic arthropod in approximately 40% of the species. Parthenogens are char- species focusing on groups with haplodiploid sex determi- acterized by larger, polewards extended geographic ranges and nation. Haplodiploidy is the sex determination system where utilize more host species than their sexual relatives. Moreover, males develop from unfertilized eggs and females from fertil- ecological attributes (i.e. the number of host species and size ized eggs. We use our database to identify ecological traits that of geographic distribution) in sexuals favor the transition to contribute to reproductive polymorphisms. and/or the success of derived parthenogenetic lineages. This Parthenogenesis evolved many more times than previ- species database sets the basis for further analyses on sexuals ously thought. We found clear evidence for parthenogene- and parthenogens that are not taxon specific. C 2017 The Author(s). Evolution Letters published by Wiley Periodicals, Inc. on behalf of Society for the Study of Evolution 1 (SSE) and European Society for Evolutionary Biology (ESEB). This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited. Evolution Letters 00-0: 1–12 VAN DER KOOI ET AL. Reproduced with Permission of Elzemiek Zinkstok, Significant Science Communication. 2 EVOLUTION LETTERS OCTOBER 2017 EVOLUTION AND COMPARATIVE ECOLOGY OF PARTHENOGENESIS Changes in reproductive modes, especially from sexual re- of parthenogenetic species however prohibits testing how genetic production to female-producing parthenogenesis (also called the- and ecological effects influence the transition rate to parthenogen- lytoky), have great evolutionary and ecological consequences esis and the persistence of parthenogenetic lineages across broad (Bell 1982), but how many times parthenogenesis evolved in dif- taxonomic groups. ferent animal taxa is unknown. Whereas parthenogenesis is rare Here, we present the first comprehensive survey of female- amongst vertebrates and absent in natural bird and mammal pop- producing parthenogenesis in haplodiploid arthropods. Hap- ulations, it occurs frequently in many species-rich invertebrate lodiploid sex determination has evolved at least 17 times inde- groups (Bell 1982; Suomalainen et al. 1987; Normark 2003). pendently, of which 15 times in arthropods (Otto and Jarne 2001). Using information mostly from vertebrates, White (1977) esti- This allows for comparative analyses across different taxonomic mated that approximately 0.1% of the described animal species groups but within a single sex-determination system. Further- reproduce by means of parthenogenesis, a frequency estimate more, approximately 12% of all animal species are haplodiploid that subsequently has been widely perpetuated (Bell 1982; Schon¨ (Bachtrog et al. 2014), and the ecologies of several haplodiploid et al. 2009). This estimate was, however, not based on a species taxonomic groups (notably insects) are well studied. In arthro- list, and vertebrates represent only a minute and nonrepresenta- pods, haplodiploidy is well known from the insect orders Hy- tive fraction (at most 1%; (May 2010)) of total animal diversity. menoptera (ants, bees, sawflies, and wasps) and Thysanoptera More importantly, parthenogenesis in vertebrates is often due to (thrips) where all species are haplodiploid, but it also occurs in tychoparthenogenesis (i.e., rare, spontaneous hatching of unfer- Hemiptera (whiteflies), a few beetle species and several groups of tilized eggs in sexual species), rather than facultative or obligate mites. We focus on obligate female-producing parthenogenesis, parthenogenesis. Given the inefficiency of tychoparthenogenesis thus excluding rare cases of facultative and cyclical partheno- (very low hatching success and low viability of offspring; re- genesis, as these reproductive systems are functionally very sim- viewed by van der Kooi and Schwander 2015), it generally plays ilar to sexual reproduction (reviewed by Neiman et al. 2014). no role in the population dynamics of a species. We do not include species characterized by paternal genome In contrast to vertebrates, the frequency of obligate partheno- elimination–where males develop from fertilized eggs, but sub- genesis in some species-rich invertebrate groups appears to be sequently eliminate their paternal chromosomes, which has re- much higher than 0.1%. Focusing on hexapods, Normark (2014) cently been reviewed elsewhere (e.g., Ross et al. 2010). When- recently pointed out that in some insect groups the overall fre- ever possible, our database includes information on the causes of quency can be orders of magnitudes higher. Indeed, studies that parthenogenesis in a lineage, especially whether parthenogenesis focused on specific invertebrate groups found high frequencies of is caused by infection with maternally inherited endosymbionts parthenogenesis, for example it was found in 15% of Megastig- (e.g., Wolbachia). Endosymbiont infection is a common cause of mus (Boivin et al. 2014) and 30% of Aphytis wasp species (De- parthenogenesis in various haplodiploid groups (Stouthamer et al. Bach 1969; Rosen and DeBach 1979). Why different taxa vary by 1990; Zchori-Fein et al. 2001). For each taxonomic group, we several orders of magnitude in the frequency of parthenogenesis calculate frequency estimates of parthenogenesis, endosymbiont- remains unknown. induced parthenogenesis, and polyploidy, and we perform com- One hypothesis that could explain the extensive variation in parative tests on ecological characteristics of sexuals and parthenogenesis frequency among taxa is that developmental and parthenogens. genetic constraints reduce the transition from sexual reproduc- tion to parthenogenesis in some cases (reviewed by Engelstaedter 2008). For example, the necessity of sperm to initiate embryo de- velopment could explain the extreme rareness of parthenogenesis Materials and Methods in vertebrates. In many invertebrates such developmental require- DATA COLLECTION ments are absent. As an example, in species with haplodiploid The species list was compiled via a thorough search through sex determination–where males develop from unfertilized eggs Google Scholar (publications until August 2016) and using previ- and females from fertilized eggs (arrhenotoky)—egg activation ously published reviews on different topics (Table 1). We started and centrosome formation is induced immediately after ovipo- with the list provided by Normark (2003) that contained 163 cases sition, independent of fertilization. However,