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. 2020 Nov 20;11(1):321–337. doi: 10.1002/ece3.7047

Repeated convergent evolution of parthenogenesis in Acariformes (Acari)

Patrick Pachl 1, Matti Uusitalo 2, Stefan Scheu 1,3, Ina Schaefer 1, Mark Maraun 1,✉
PMCID: PMC7790623  PMID: 33437432

Abstract

The existence of old species‐rich parthenogenetic taxa is a conundrum in evolutionary biology. Such taxa point to ancient parthenogenetic radiations resulting in morphologically distinct species. Ancient parthenogenetic taxa have been proposed to exist in bdelloid rotifers, darwinulid ostracods, and in several taxa of acariform mites (Acariformes, Acari), especially in oribatid mites (Oribatida, Acari). Here, we investigate the diversification of Acariformes and their ancestral mode of reproduction using 18S rRNA. Because parthenogenetic taxa tend to be more frequent in phylogenetically old taxa of Acariformes, we sequenced a wide range of members of this taxon, including early‐derivative taxa of Prostigmata, Astigmata, Endeostigmata, and Oribatida. Ancestral character state reconstruction indicated that (a) Acariformes as well as Oribatida evolved from a sexual ancestor, (b) the primary mode of reproduction during evolution of Acariformes was sexual; however, species‐rich parthenogenetic taxa radiated independently at least four times (in Brachychthonioidea (Oribatida), Enarthronota (Oribatida), and twice in Nothrina (Oribatida), (c) parthenogenesis additionally evolved frequently in species‐poor taxa, for example, Tectocepheus, Oppiella, Rostrozetes, Limnozetes, and Atropacarus, and (d) sexual reproduction likely re‐evolved at least three times from species‐rich parthenogenetic clusters, in Crotonia (Nothrina), in Mesoplophora/Apoplophora (Mesoplophoridae, Enarthronota), and in Sphaerochthonius/Prototritia (Protoplophoridae, Enarthronota). We discuss possible reasons that favored the frequent diversification of parthenogenetic taxa including the continuous long‐term availability of dead organic matter resources as well as generalist feeding of species as indicated by natural variations in stable isotope ratios.

Keywords: backbone, diversification, evolution, mites, Oribatida, phylogeny, sex

We investigated the radiation of Acariformes and reconstructed their ancestral mode of reproduction using 18S rDNA. We found that (a) Acariformes as well as Oribatida evolved from a sexual ancestor, (b) species‐rich parthenogenetic taxa radiated independently at least four times in Acariformes, (c) parthenogenesis additionally evolved frequently in species‐poor taxa/genera and (d) sexual reproduction likely re‐evolved at least three times from species‐rich parthenogenetic clusters

graphic file with name ECE3-11-321-g002.jpg

1. INTRODUCTION

One of the unsolved enigmas in evolutionary biology is the dominance of sexual reproduction in animal taxa (Brandeis, 2018; Burke & Bonduriansky, 2017; Otto, 2003; Williams, 1975). Despite the many disadvantages of sexual reproduction, including dilution of the genome, breakup of favorable gene combinations, production of males, exposure to predators during courtship and copulation, as well as the transmission of sexual diseases (Bell, 1982; Lehtonen et al., 2013; Maynard Smith, 1978), there must be short‐term advantages of sexual reproduction that prevent the establishment and spread of parthenogenetic lineages (Hartfield & Keightley, 2012). To understand the dominance of sexual reproduction in the animal kingdom, it is instructive to investigate exceptions, that is, animal species that reproduce via parthenogenesis, in particular those persisting for long periods of time (Neiman et al., 2009). Such “ancient asexual scandals” (Maynard Smith, 1978) include bdelloid rotifers, darwinulid ostracods, and several taxa of oribatid mites (Oribatida, Acariformes) (Bode et al., 2010; Brandt et al., 2017; Flot et al., 2013; Ricci, 2017; Schaefer et al., 2010). However, recently it has been shown that bdelloid rotifers engage in some kind of non‐canonical sex (Debortoli et al., 2016) and that there are males in darwinulid ostracods, although very rare (Smith et al., 2006), rendering Oribatida among the last candidates for the evolution and diversification of parthenogenetic taxa (Schwander, 2016). Unfortunately, the phylogeny, evolution, and diversification of Oribatida and Acariformes in general are not well understood, mainly due to the large number of taxa and lineages in this group (Arribas et al., 2019; Maraun et al., 2003, 2004; Pachl et al., 2012; Palmer & Norton, 1991; Schaefer & Caruso, 2019; Schaefer et al., 2010).

Parthenogenetic diversifications are rare events in evolution (Heethoff et al., 2007; Maraun et al., 2004). First, due to the lack of adaptive potential, parthenogenetic taxa have been assumed to be doomed to extinction (Maynard Smith, 1971); however, parthenogenetic taxa may be able to adapt to their environment via phenotypic plasticity and epigenetic mechanisms (Gutekunst et al., 2018). Second, diversification of parthenogenetic lineages appears paradoxical because mechanisms allowing the evolution of morphologically distinct species without sex remain elusive. While sexual taxa are linked via a common gene pool, in parthenogenetic taxa, each lineage evolves independently. Why parthenogenetic Oribatida species form morphologically coherent units therefore remains enigmatic. Rather than morphologically uniform lineages, one may expect a plethora of transition forms to exist in parthenogenetic taxa. However, some species‐rich and monophyletic parthenogenetic taxa, which include morphologically distinct species, likely exist in Oribatida (Domes et al., 2007; Norton & Palmer, 1991; Palmer & Norton, 1991). Those species‐rich monophyletic taxa are unique in the animal kingdom and may therefore essentially contribute to our understanding of the long‐term persistence and diversification of parthenogenetic lineages in animals.

Even more surprising (and possibly more rare) than parthenogenetic diversification is the re‐evolution of sex from parthenogenetic ancestors. There are only a few known instances, one in the plant species Hieracium pilosella, the mouse‐ear hawkweed (Asteraceae; Chapman et al., 2003), one in the mite genus Crotonia (Oribatida; Domes et al., 2007) and another in ostracods (Horne, 2010). The circumstances that allow or even trigger the re‐evolution of sex are not known, but their cytology may contribute to this pattern. Automictic thelytokous taxa, which still undergo meiosis, may more easily re‐evolve sex than apomicts that lost meiosis entirely. Also, ecological conditions might favor sexual reproduction and therefore the re‐evolution of sex, for example, the transition from plentiful to scarce and heterogeneously distributed resources during evolution (Scheu & Drossel, 2007).

Acariformes, particularly Oribatida, are perfect model organisms to study parthenogenetic radiations and re‐evolution of sex. They include an exceptional high proportion of parthenogenetic taxa, with many of them being phylogenetically old and having radiated in the Carboniferous or earlier (Heethoff et al., 2009; Pachl et al., 2017; Schaefer et al., 2010). Especially the early‐derivative taxa in Oribatida, such as Enarthronota and Nothrina, include many parthenogenetic species, which is surprising because parthenogenesis is often assumed to lack the adaptive potential to persist in the long term (Maynard Smith, 1971, 1978).

Here, we investigated the phylogeny of Acariformes (Prostigmata, Astigmata, Endeostigmata, and Oribatida), with a focus on early‐derivative Oribatida and inferred their ancestral mode of reproduction (sexual vs. parthenogenetic). The phylogenetic relationships among early‐derivative lineages of Oribatida and their monophyly are controversial (Arribas et al., 2019). To independently resolve phylogenetic relationships, we used sequences of 18S rRNA, a gene that allows resolving deep splits in Oribatida (Schaefer et al., 2010) and other Acari; for example, it has been used to unveil the evolution of Parasitiformes (Klompen et al., 2007), the origin and higher‐level diversification of Acariformes (in combination with LSU; Pepato & Klimov, 2015), and the phylogenetic position of the Eriophyoidea within Acariformes (Xue et al., 2017). Importantly, Oribatida may include a wide range of taxa with equivocal phylogenetic position, such as Astigmata and Endeostigmata, and represent the major taxa of Acariformes.

We hypothesized that (a) the ancestral mode of reproduction (i.e., the backbone of the phylogenetic tree) in Acariformes and Oribatida is sexual because the alternative hypothesis is unlikely. If the backbone would have been parthenogenetic, sexual reproduction would have re‐evolved several times, which is very unlikely. If the ancestral mode of reproduction had been sexual, we furthermore hypothesized that (b) parthenogenesis evolved several times independently within Acariformes, and that (c) parthenogenetic taxa radiated into several distinct morphological species. Finally, because few species‐rich parthenogenetic taxa include sexual species we hypothesized that (d) sexual reproduction re‐evolved occasionally in Acariformes.

2. MATERIALS AND METHODS

2.1. Taxon sampling

In total, 130 species comprising 119 Acariformes (81 Oribatida, 11 Endeostigmata, 13 Astigmata, 14 Prostigmata) and five Parasitiformes, with six non‐Acari Arachnida as outgroup taxa, were included in the dataset. The 81 Oribatida included representatives of the six major phylogenetic groups (26 Brachypylina, 15 Nothrina, 22 Enarthronota, 11 Mixonomata, five Palaeosomata, and two Parhyposomata). Of these, 69 Oribatida were identified at species level and twelve at genus level. Sixteen taxa were newly sampled and sequenced for our study; all other sequences were obtained from NCBI. New species/specimens were extracted by using a heat gradient (Kempson et al., 1963), and mites were determined using relevant taxonomic literature, particularly Balogh and Balogh (1988, 1990, 2002) and Weigmann (2006). Specimens were collected from tropical montane rainforests in southern Ecuador (Illig et al., 2010), temperate forests in central Germany (Erdmann et al., 2012) and various locations in the United States of America, and from several sites all over the world (Table 1). Oribatida species were assigned to higher taxonomic groups according to the classification of Norton and Behan‐Pelletier (2009). Modes of reproduction (i.e., sexual or parthenogenetic) were taken from literature (Maraun et al., 2019; Norton et al., 1993). Mode of reproduction is known from rearing experiments and sex ratios, but in part also was ascribed based on the reproductive mode of sister taxa. Since biological species concepts sensu Mayr (1963) do not apply for parthenogenetic species, we adopted the morphological species concept of Cronquist (1978).

TABLE 1.

Species name, phylogenetic affiliation, reproductive mode, and GenBank accession numbers of Acariformes, other Chelicerate taxa, and outgroups

Species/genus Family Superfamily Taxon/Supercohort Reproductive mode (coded for MESQUITE) GenBank accession nrs. 18S
Carcinoscorpius rotundicauda (Pocock, 1902) Xiphosura (outgroup) Sexual HQ588739
Limulus polyphemus (Linnaeus, 1758) Xiphosura (outgroup) Sexual L81949
Chelifer cancroides (Linnaeus, 1758) Pseudoscorpiones Sexual KT354350
Ellingsenius indicus (Chamberlin, 1932) Pseudoscorpiones Sexual KT354353
Eusimonia wunderlichi (Kraepelin, 1899) Solifugae Sexual U29492
Gluvia dorsalis (C.L. Koch, 1842) Solifugae Sexual AF007103
Neocarus sp. (Chamberlin & Mulaik, 1942) Opilioacarida Sexual KP276467
Opilioacarus texanus (Chamberlin & Mulak, 1942) Opilioacarida Sexual AF115375
Amblyomma sphenodonti (Dumbleton, 1943) Ixodidae Sexual DQ507238
Pergamasus canestrinii (Berlese, 1884) Parasitidae Parasitoidea Mesostigmata Sexual AY620934
Trachytes sp. (Michael, 1894) Trachytidae Polyaspidoidea Mesostigmata Sexual MT683118
Anystis sp. (Heyden, 1826) Anystidae Anystoidea Trombidiformes Sexual KP325052
Bdellodes sp. (Oudemans, 1937) Bdellidae Bdelloidea Trombidiformes Sexual HM070358
Spinibdella sp. (Thor, 1930) Bdellidae Bdelloidea Trombidiformes Sexual HM070368
Microcaeculus sp. (Franz, 1952) Caeculidae Caeculoidea Trombidiformes Sexual AF287232
Neochelacheles messersmithi (Smiley & Williams, 1972) Cheyletidae Cheyletoidea Trombidiformes Sexual AY620908
Balaustium sp. (Von Heyden, 1826) Erythraeidae Erythraeoidea Trombidiformes Sexual EF203775
Eupodes sp. (Koch, 1835) Eupodidae Eupodoidea Trombidiformes Sexual HM070365
Diplothrombium sp. (Berlese, 1910) Johnstonianidae Trombiculoidea Trombidiformes Sexual KM100930
Labidostomma sp. (Kramer, 1879) Labidostomatidae Labidostomatoidea Trombidiformes Sexual EF203774
Tanytydeus sp. (Theron et al, 1969) Paratydeidae Paratydeoidea Trombidiformes Sexual KY922147
Eotetranychus uchidai (Ehara, 1956) Tetranychidae Tetranychoidea Trombidiformes Sexual AB926274
Oligonychus rubicundus (Ehara, 1971) Tetranychidae Tetranychoidea Trombidiformes Sexual AB926290
Tetranychus urticae (Koch, 1836) Tetranychidae Tetranychoidea Trombidiformes Sexual AB926313
Yezonychus sapporensis (Ehara, 1978) Tetranychidae Tetranychoidea Trombidiformes Sexual AB926258
Acarus gracilis (Hughes, 1975) Acaridae Acaroidea Astigmata Sexual EF203769
Aleuroglyphus ovatus (Troupeau, 1879) Acaridae Acaroidea Astigmata Sexual EF203770
Naiadacarus arboricola (Fashing, 1974) Acaridae Acaroidea Astigmata Sexual JQ000114
Tyrophagus brevicrinatus (Robertson, 1959) Acaridae Acaroidea Astigmata Sexual MT683111
Austroglycyphagus (=Glycycometus) geniculatus (Vitzthum, 1919) Aeroglyphidae Glycyphagoidea Astigmata Sexual EF203773
Arrunsithiana nr. spicantis (Summers and Schuster, 1979) Canestriniidae Canestrinioidea Astigmata Sexual JQ000086
Dermacarus tamiasciuri (Rupes, Yunker, and Wilson, 1971) Canestriniidae Canestrinioidea Astigmata Sexual KP325070
Carpoglyphus lactis (Linnaeus, 1767) Carpoglyphidae Hemisarcoptoidea Astigmata Sexual EF203772
Lepidoglyphus destructor (Schrank, 1781) Glycyphagidae Glycyphagoidea Astigmata Sexual EF203771
Nanacarus sp. (Oudemans, 1902) Hemisarcoptidae Hemisarcoptoidea Astigmata Sexual JQ000068
Histiostoma feroniarum (Dufour, 1839) Histiostomatidae Histiostomatoidea Astigmata Sexual GQ864328
Neottialges vitzthumi (Fain, 1967) Hypoderatidae Hypoderatoidea Astigmata Sexual JQ000122
Dermatophagoides pteronyssinus (Trouessart, 1898) Pyroglyphidae Analgoidea Astigmata Sexual MT683110
Alicorhagia sp. (Berlese, 1910) Alicorhagiidae Endeostigmata Parthenogenetic EU675633
Alycus sp. (C. L. Koch, 1842) Alycidae Endeostigmata Sexual MT683115
Bimichaelia sp. (Thor, 1902) Alycidae Endeostigmata Sexual KY922112
Pachygnathus (Dugès, 1834) Alycidae Endeostigmata Sexual KY922115
Hybalicus sp. (Berlese, 1913) Hybalicidae Endeostigmata Parthenogenetic MT683116
Micropsammus sp. (Coineau & Théron, 1983) Micropsammidae Endeostigmata Sexual KY922132
Nanorchestes sp. (Topsent & Trouessart, 1890) Nanorchestidae Endeostigmata Sexual KP325043
Cunliffea sp. (Schubart, 1973) Nematalycidae Endeostigmata Sexual KY922118
Gordialycus sp. (Coineau, Fize and Delamare Deboutteville, 1967) Nematalycidae Endeostigmata Sexual KY922131
Oehserchestidae sp. (Kethley, 1977) Terpnacaridae Endeostigmata Sexual KP325049
Terpnacarus gibbosus (Womersley, 1944) Terpnacaridae Endeostigmata Parthenogenetic AY620904
Stomacarus ligamentifer (Hammer, 1967) Archeonothridae Acaronychoidea Oribatida/Palaeosomatides Sexual EU433992
Zachvatkinella sp. (Lange, 1954) Archeonothridae Acaronychoidea Oribatida/Palaeosomatides Sexual EF203776
Beklemishevia galeodula (Zachvatkin, 1945) Ctenacaridae Ctenacaroidea Oribatida/Palaeosomatides Sexual KP325051
Ctenacarus araneola (Grandjean, 1932) Ctenacaridae Ctenacaroidea Oribatida/Palaeosomatides Sexual EU433991
Palaeacarus hystricinus (Trägardh, 1932) Palaeacaridae Palaeacaroidea Oribatida/Palaeosomatides Parthenogenetic EF204472
Atopochthonius artiodactylus (Grandjean, 1949) Atopochthoniidae Atopochthonioidea Oribatida/Enarthronotides Parthenogenetic EU432216
Brachychthonius bimaculatus (Willmann, 1936) Brachychthonidae Brachychthonioidea Oribatida/Enarthronotides Parthenogenetic MK630360
Liochthonius peduncularius (Strenzke, 1951) Brachychthoniidae Brachychthonioidea Oribatida/Enarthronotides Parthenogenetic MK630365
Neoliochthonius piluliferus (Forsslund, 1942) Brachychthoniidae Brachychthonioidea Oribatida/Enarthronotides Parthenogenetic MK630366
Cosmochthonius lanatus (Michael, 1885) Cosmochthoniidae Protoplophoroidea Oribatida/Enarthronotides Sexual JN585919
Eniochthonius minutissimus (Berlese, 1904) Eniochthoniidae Hypochthonioidea Oribatida/Enarthronotides Parthenogenetic KR081609
Haplochthonius simplex (Willmann, 1930) Haplochthoniidae Protoplophoroidea Oribatida/Enarthronotides Parthenogenetic EU675634
Hypochthonius rufulus (Koch, 1835) Hypochthoniidae Hypochthonioidea Oribatida/Enarthronotides Parthenogenetic KR081618
Lohmannia banksi (Norton, Metz & Sharma, 1978) Lohmanniidae Hypochthonioidea Oribatida/Enarthronotides Parthenogenetic AF022036
Meristacarus sp. (Grandjean, 1934) Lohmanniidae Hypochthonioidea Oribatida/Enarthronotides Parthenogenetic KP276478
Meristolohmannia meristacaroides (Balogh & Mahunka, 1966) Lohmanniidae Hypochthonioidea Oribatida/Enarthronotides Parthenogenetic AY620905
Mixacarus brevipes (Banks, 1947) Lohmanniidae Hypochthonioidea Oribatida/Enarthronotides Parthenogenetic JN585913
Nesiacarus granulatus (Hammer, 1972) Lohmanniidae Hypochthonioidea Oribatida/Enarthronotides Parthenogenetic JN585914
Apoplophora sp. (Aoki, 1980) Mesoplophoridae Hypochthonioidea Oribatida/Enarthronotides Sexual JN585917
Archoplophora rostralis (Willmann, 1930) Mesoplophoridae Hypochthonioidea Oribatida/Enarthronotides Parthenogenetic JN585918
Mesoplophora cubana (Calugar & Vasiliu, 1977) Mesoplophoridae Hypochthonioidea Oribatida/Enarthronotides Sexual EU432217
Nanohystrix hammerae (Norton & Fuangarworn, 2015) Nanohystricidae Heterochthonioidea Oribatida/Enarthronotides Sexual MT683114
Paralycus sp. (Womersley, 1944) Pediculochelidae Cosmochthonioidea Oribatida/Enarthronotides Parthenogenetic KY922209
Prototritia major (Jacot, 1933) Protoplophoridae Protoplophoroidea Oribatida/Enarthronotides Sexual JN585915
Pterochthonius angelus (Berlese, 1910) Pterochthoniidae Atopochthonioidea Oribatida/Enarthronotides Parthenogenetic EU432214
Sphaerochthonius sp. (Berlese, 1910) Sphaerochthoniidae Protoplophoroidea Oribatida/Enarthronotides Sexual JN585916
Gozmanyina majestus (Marshall & Reeves, 1971) Trichthoniidae Heterochthonioidea Oribatida/Enarthronotides Parthenogenetic EU433993
Gehypochtonius urticinus (Berlese, 1910) Gehypochthoniidae Parhypochthonioidea Oribatida/Parhyposomatides Parthenogenetic EU433994
Parhypochthonius aphidinus (Berlese, 1904) Parhypochthoniidae Parhypochthonioidea Oribatida/Parhyposomatides Parthenogenetic EU432215
Collohmannia gigantea (Sellnick, 1922) Collohmanniidae Collohmannioidea Oribatida/Mixonomatides Sexual KR081604
Epilohmannia sp. (Berlese, 1910) Epilohmannidae Epilohmannioidea Oribatida/Mixonomatides Sexual EU432213
Eulohmannia ribagai (Berlese, 1910) Eulohmanniidae Eulohmannioidea Oribatida/Mixonomatides Parthenogenetic EU432211
Acrotritia (=Rhysotritia) duplicata (Grandjean, 1953) Euphthiracaridae Euphthiracaroidea Oribatida/Mixonomatides Parthenogenetic EF091417
Nehypochthonius porosus (Norton & Metz, 1980) Nehypochthoniidae Nehyochthonioidea Oribatida/Mixonomatides Parthenogenetic AF022038
Indotritia krakatauensis (Sellnick, 1923) Oribotritiidae Euphthiracaroidea Oribatida/Mixonomatides Sexual JN85920
Perlohmannia sp. (Berlese, 1916) Perlohmanniidae Perlohmannioidea Oribatida/Mixonomatides Sexual EU432212
Atropacarus striculus (Koch, 1835) Phthiracaridae Phthiracaroidea Oribatida/Mixonomatides Parthenogenetic EF091416
Phthiracarus sp. (Perty, 1841) Phthiracaridae Phthiracaroidea Oribatida/Mixonomatides Sexual KR081629
Steganacarus magnus (Nicolet, 1855) Phthiracaridae Phthiracaroidea Oribatida/Mixonomatides Sexual AF022040
Synichotritia caroli (Walker, 1965) Synichotritiidae Euphthiracaroidea Oribatida/Mixonomatides Sexual MT683117
Camisia segnis (Hermann, 1804) Camisiidae Crotonioidea Oribatida/Nothrina Parthenogenetic EU432209
Platynothrus peltifer (Koch, 1839) Camisiidae Crotonioidea Oribatida/Nothrina Parthenogenetic EF091422
Crotonia brachyrostrum (Hammer, 1966) Crotoniidae Crotonioidea Oribatida/Nothrina Sexual EF081303
Hermannia gibba (Koch, 1839) Hermanniidae Crotonioidea Oribatida/Nothrina Sexual EF091426
Trimalaconothrus sp. (Berlese, 1916) Malaconothridae Crotonioidea Oribatida/Nothrina Parthenogenetic EU432210
Masthermannia sp. (Berlese, 1913) Nanhermanniidae Crotonioidea Oribatida/Nothrina Parthenogenetic KY922217
Nanhermannia nana (Nicolet, 1855) Nanhermanniidae Crotonioidea Oribatida/Nothrina Parthenogenetic KR081624
Nothrus truncatus (Banks, 1895) Nothridae Crotonioidea Oribatida/Nothrina Parthenogenetic EF081306
Novonothrus flagellatus (Hammer, 1966) Nothridae Crotonioidea Oribatida/Nothrina Sexual EF081307
Afronothrus sp. (Wallwork, 1961) Trhypochthoniidae Crotonioidea Oribatida/Nothrina Parthenogenetic EU152476
Allonothrus russeolus (Wallwork, 1960) Trhypochthoniidae Crotonioidea Oribatida/Nothrina Parthenogenetic AF022025
Archegozetes longisetosus (Aoki, 1965) Trhypochthoniidae Crotonioidea Oribatida/Nothrina Parthenogenetic HQ661379
Mainothrus badius (Berlese, 1905) Trhypochthoniidae Crotonioidea Oribatida/Nothrina Parthenogenetic EF081301
Mucronothrus nasalis (Willmann, 1929) Trhypochthoniidae Crotonioidea Oribatida/Nothrina Parthenogenetic EF081299
Trhypochthonius americanus (Ewing, 1908) Trhypochthoniidae Crotonioidea Oribatida/Nothrina Parthenogenetic JQ000046
Achipteria coleoptrata (Linnaeus, 1758) Achipteriidae Achipterioidea Oribatida/Brachypylina Sexual EF091418
Caleremaeus monilipes (Michael, 1882) Caleremaeidae Ameroidea Oribatida/Brachypylina Sexual MK630361
Carabodes subarcticus (Trägårdh, 1902) Carabodidae Carabodoidea Oribatida/Brachypylina Sexual EF091429
Cepheus dentatus (Michael, 1888) Cepheidae Cepheoidea Oribatida/Brachypylina Sexual MK630354
Oromurcia sudetica (Willmann, 1939) Ceratozetidae Ceratozetoidea Oribatida/Brachypylina Sexual EU432194
Scapheremaeus palustris (Sellnick, 1924) Cymbaeremaeidae Cymbaeremaeoidea Oribatida/Brachypylina Sexual EU433989
Eueremaeus oblongus (Koch, 1835) Eremaeidae Eremaeoidea Oribatida/Brachypylina Sexual EU432205
Eremaeozetes sp. (Berlese, 1913) Eremaeozetidae Eremaeozetoidea Oribatida/Brachypylina Sexual EU432187
Galumna lanceata (Oudemans, 1900) Galumnidae Galumnoidea Oribatida/Brachypylina Sexual KX397630
Gymnodamaeus bicostatus (Koch, 1835) Gymnodamaeidae Plateremaeoidea Oribatida/Brachypylina Sexual KR081614
Rostrozetes ovulum (Berlese, 1908) Haplozetidae Oripodoidea Oribatida/Brachypylina Parthenogenetic HM070342
Humerobates rostrolamellatus (Grandjean, 1936) Humerobatidae Ceratozetoidea Oribatida/Brachypylina Sexual EU432196
Hydrozetes thienemanni (Strenzke, 1943) Hydrozetidae Hydrozetoidea Oribatida/Brachypylina Sexual KX397633
Xenillus discrepans (Hermann, 1804) Liacaridae Gustavioidea Oribatida/Brachypylina Sexual EU432203
Limnozetes foveolatus (Willmann, 1939) Limnozetidae Hydrozetoidea Oribatida/Brachypylina Parthenogenetic KX397634
Mycobates tridactylus (Willmann, 1929) Mycobatidae Ceratozetoidea Oribatida/Brachypylina Sexual MT683112
Poroliodes farinosus (Koch, 1839) Neoliodidae Neoliodioidea Oribatida/Brachypylina Sexual EF203779
Oppiella nova (Oudemans, 1902) Oppiidae Oppioidea Oribatida/Brachypylina Parthenogenetic KR081626
Liebstadia humerata (Sellnick, 1928) Oribatulidae Oripodoidea Oribatida/Brachypylina Sexual KR081620
Oribatula tibialis (Nicolet, 1855) Oribatulidae Oripodoidea Oribatida/Brachypylina Sexual EU433990
Ceratoppia bipilis (Hermann, 1804) Peloppiidae Gustavioidea Oribatida/Brachypylina Sexual EU432204
Eupelops plicatus (Koch, 1835) Phenopelopidae Phenopelopoidea Oribatida/Brachypylina Sexual EF091419
Scheloribates ascendens (Weigmann & Wunderle, 1990) Scheloribatidae Oripodoidea Oribatida/Brachypylina Sexual MT683113
Tectocepheus sarekensis (Trägårdh, 1910) Tectocepheidae Tectocepheoidea Oribatida/Brachypylina Parthenogenetic EF093776
Hafenrefferia gilvipes (Koch, 1839) Tenuialidae Gustavioidea Oribatida/Brachypylina Sexual MK630363
Banksinoma lanceolata (Michael, 1885) Thyrisomidae Oppioidea Oribatida/Brachypylina Sexual MK630359
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2.2. DNA extraction and PCR

Genomic DNA was extracted from single individuals using the DNeasy Blood and Tissue Kit (Qiagen) with silica membrane columns and protease K from Genaxxon (25 mM; Genaxxon BioScience). Amplification of target genes was performed in 25 µl volume. Primers for 18S rDNA were 5′‐TAC CTG GTT GAT CCT GCC AG‐3′ (18Sforward) and 5′‐AAT GAT CCT TCC GCA GGT TCA C‐3′ (18Sreverse) (Domes et al., 2007). The 18S rDNA fragment was amplified at 57°C using standard PCR protocols. PCR products were sequenced at Göttingen Genomics Laboratory (Institute of Microbiology and Genetics, University of Göttingen, Germany), using the additional sequencing primers 18S554f 5′‐AAG TCT GGT GCC AGC AGC CGC‐3′, 18S1282r 5′‐TCA CTC CAC CAA CTA AGA ACG GC‐3′, 18S1150f 5′‐ATT GAC GGA AGG GCA CCA CCA G‐3′ and 18S614r 5′‐TCC AAC TAC GAG CTT TTT AAC C‐3′ (Domes et al., 2007). Sequences MK630354, MK630359‐61, MK630363, MK630365‐66, and MT683110‐18 were generated for this study (in total 16 sequences; Table 1); all other sequences were obtained from NCBI. We used the 18S rRNA gene since no other reliable genes for reconstructing the phylogeny of Acariformes are available.

2.3. Sequence alignment and phylogenetic analysis

The 18S rDNA gene sequences generated for this study were assembled and edited in Sequencher 5.1 (Gene Codes Corporation); ambiguous positions were corrected using the chromatograms. The final alignment of 130 sequences had a total length of 2,455 characters; the shortest sequence had 1,468 bp (Pergamasus canestrinii, Mesostigmata), the longest 1,897 bp (Haplochthonius simplex, Enarthronota). Sequences of the alignment were trimmed to the shortest sequence downloaded from NCBI. Sequences were aligned in ClustalX 2.1 (Larkin et al., 2007). Several gap opening and gap extension parameters were tested and used for Maximum‐Likelihood reconstruction in R v3.6 (R Core Team, 2018) using the pml function of the phangorn package (Schliep, 2011). The parameters for gap opening = 20 and gap extension = 0.1 resulted in the best‐supported phylogeny. Partitioning of sequences into conserved and variable regions and applying different alignment parameters and models of sequence evolution did not improve the phylogenetic trees or bootstraps. The final phylogenetic tree was constructed with IQ‐TREE v1.6 (Nguyen et al., 2015) using ModelFinder (Kalyaanamoorthy et al., 2017) and ultrafast bootstrap (Hoang et al., 2018) with 1,000 bootstrap replicates and setting Limulus polyphemus (Xiphosura) as outgroup taxon. To test for the robustness of the ML tree, we also calculated trees in MrBayes using the same settings (lset nst = 6 rates = gammainv) and the same outgroup. We ran the mcmc chain for 5 million generations, with a sample frequency of 5,000 and a burnin of 25%. The resulting tree had the same topology as the ML tree, except that nodes with lower bootstrap support were not resolved and were displayed as polytomies in the Bayesian tree (Figure S1).

2.4. Inferring the ancestral reproductive mode

We used Mesquite 3.61 (Maddison & Maddison, 2019) to map the mode of reproduction as a character on the phylogenetic tree. Character history was traced using parsimony to infer patterns of the ancestral state of reproduction using the symmetrical Mk1 (Markov k‐state 1 parameter) model using the parameters 1, 5, and 10 for character change and asymmetrical models with higher rates for the loss of sex (5:1, 10:1). The ancestral character history did not differ among these models. Likelihood analyses using the same parameter as for the asymmetrical model resulted in fully ambiguous backbone. Because reproductive modes are complex traits, we continue with the results of the parsimony inference. The Maximum‐Likelihood tree generated by IQ‐Tree provided the topology, and the present‐day reproductive mode of investigated species was coded as sexual or parthenogenetic.

3. RESULTS

3.1. Ancestral mode of reproduction and reproductive mode during evolution

Ancestral character state reconstruction indicated that the plesiomorphic state of reproduction in Acariformes and in Oribatida was sexual (Figure 1). Outgroup taxa (mainly Prostigmata) were mainly sexual. In general, Endeostigmata clustered at separate positions in the phylogenetic tree, suggesting that the taxon is not monophyletic. Ancestral character state reconstruction further indicated that the mode of reproduction of Oribatida during evolution was mainly sexual; however, some remained uncertainty at intermediate positions of the backbone (Figure 1).

FIGURE 1.

FIGURE 1

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Maximum‐likelihood tree of Acariformes based on 18S rRNA gene of Acariformes including three other arachnid taxa (Parasitiformes, Pseudoscorpiones, Solifugae) and two outgroup taxa (Xiphosura). Numbers at nodes represent bootstrap supports (1,000 replicates). Ancestral character state reconstruction of the reproductive mode (sexual = black, parthenogenetic = red) was carried out using Maximum Parsimony in Mesquite (Maddison & Maddison, 2019). Oriba: Oribatida, Endeo: Endostigmata, Prost: Prostigmata, Opili: Opilioacariformes, Paras: Parasitiformes, Pseud: Pseudoscorpiones, Solif: Solifugae, Xipho: Xiphosura

3.2. Convergent evolution of parthenogenesis

According to the ancestral character state reconstruction (Figure 1), the sampled species represent at least 17 independent evolutionary events of thelytoky. The number, however, remains ambiguous as the character state reconstruction of the mode of reproduction in some cases was only weakly supported. Notably, lineages that switched to thelytoky included lineages with only one or few species, such as Limnozetes, Tectocepheus, Rostrozetes, and Oppiella nova in Brachypylina, Nehypochthonius porosus, Atropacarus, and Acrotritia in Mixonomata, Haplochthonius in Enarthronota, and Palaeacarus in Palaeosomata, but also species‐rich clades, such as Brachychthonioidea, Nothrina, and Enarthronota.

3.3. Re‐evolution of sex

Ancestral character state reconstruction indicated that there are three independent cases of re‐evolution of sex in the examined Oribatida, that is, in Crotonia brachyrostrum (Nothrina), in Mesoplophora/Apoplophora (Mesoplophoridae, Enarthronota), and in Sphaerochthonius/Prototritia (Protoplophoridae, Enarthronota) (Figure 1). Two of these cases were strongly supported by high bootstrap values (99 for Crotonia brachyrostrum, 100 for Sphaerochthonius/Prototritia), one was weakly supported (54 for Mesoplophora/Apoplophora; Figure 1).

4. DISCUSSION

The oribatid mite phylogenetic tree based on the 18S rRNA gene was generally well‐resolved and supported by moderate to high bootstrap values. Additionally, many of its monophyletic taxa (as indicated in Figure 1) agree with morphologically well‐supported taxa (Dabert et al., 2010; Norton & Behan‐Pelletier, 2009; Schaefer et al., 2010; Schäffer et al., 2010; Weigmann, 2006). Taxa which were assumed to be paraphyletic based on morphological characters (e.g., Nothrina, Mixonomata) were also not monophyletic in the tree. Oribatida were also not monophyletic but included Astigmata and several species of Endeostigmata (Norton, 1994; O'Connor, 1984). The generally high bootstrap values, and the close matching with morphologically based evidence of monophyletic and paraphyletic groupings support the overall validity of the tree for inferring the ancestral state of reproduction of Acariformes. However, we are aware that a single locus may not allow to accurately represent the phylogeny of Acariformes and that uncertainties remain about the assignment of the reproductive mode at weakly supported nodes; information on more genes is needed to resolve the phylogeny of Acariformes in particular at ambiguous nodes.

4.1. Ancestral mode of reproduction

The phylogenetic tree based on 18S rDNA indicates that the ancestral reproductive mode in Acariformes and in Oribatida is sexual. Astigmata also are exclusively sexual and presumably form a monophyletic clade within Oribatida (Klimov & O'Connor, 2013; Pepato & Klimov, 2015). However, the sister taxon of Astigmata still is unclear, because its phylogenetic position in molecular studies was sensitive to taxon sampling and markers (Dabert et al., 2010; Domes et al., 2007; Klimov & O'Connor, 2013; Pepato & Klimov, 2015). In this study, Astigmata derived with weak support within Brachychthoniidae. Genome data of mites may eventually solve the phylogenetic position of Astigmata among Acariformes. Overall, the many parthenogenetic taxa in Acariformes and in Oribatida with their scattered distribution in the phylogenetic tree support the hypothesis that sex was lost many times during the evolution of Acariformes. Parthenogenetic taxa near the base of the Acariformes phylogeny, for example,. Alicorhagia sp. or Terpnacarus gibbosus, presumably represent offshoots that evolved parthenogenesis independently. Additionally, the early‐derivative taxa in Oribatida, that is, Palaeosomata, were also sexual further supporting the view that the ancestral reproductive mode in Oribatida was sexual. Overall, our findings indicate that parthenogenesis evolved not at the beginning but later during the evolution of Oribatida.

4.2. Reproductive mode of the backbone

The most parsimonious explanation of the ancestral character state reconstruction of the reproductive mode in Acariformes and Oribatida is that their ancestral mode of reproduction was sexual, indicating that this mode of reproduction was maintained throughout their evolution. However, the ancestral character state reconstruction remains somewhat ambiguous due to many parthenogenetic lineages in the tree. Considering that there are only few cases of the re‐evolution of sex (Chapman et al., 2003; Domes et al., 2007; Horne, 2010), whereas parthenogenesis presumably evolved thousands of times (Bell, 1982; Neiman et al., 2014), a parthenogenetic backbone is very unlikely.

4.3. Multiple origin and diversification of parthenogenetic taxa

Results of our study confirmed earlier conclusions that parthenogenesis in Oribatida evolved multiple times (Krause et al., 2016; Norton & Palmer, 1991; Pachl et al., 2012, 2017). This supports the suggestion that sex may be lost easily during evolution (Simon et al., 2003), although the routes to parthenogenesis from sexual ancestors are manifold (Bell, 1982; Suomalainen et al., 1987). The frequent and convergent transition from sexual to parthenogenetic reproduction in Oribatida thus may not be surprising; it also occurred, for example, in the lepidopteran species Dahlica triquetrella (Elzinga et al., 2013), in the lizard genus Leiolepis (Grismer et al., 2014), in the ostracod species Eucypris virens (Bode et al., 2010), in grasshopper and gecko species (Kearney et al., 2006), and in Timema stick insects (Schwander & Crespi, 2009). However, the benefits of the loss of sex are controversially discussed and include hybrid vigor (=heterosis) (Vrijenhoek, 1998), extension of the geographical range associated with a “general purpose genotype” (Lynch, 1984), enhanced survival of harsh environmental conditions (Kearney et al., 2006), or faster exploitation of unlimited resources (Scheu & Drossel, 2007). For Oribatida, the latter possibly plays a major role because high densities of Oribatida (an indication that resources are plentiful) correlate with high frequency of parthenogenetic species and individuals (Maraun et al., 2012, 2019).

Despite the evolutionary benefits of parthenogenesis, diversification of a parthenogenetic lineage into morphologically distinct species is enigmatic and perhaps unique for Oribatida. The phylogeny of Oribatida presented in this study supports earlier views (Heethoff et al., 2009; Palmer & Norton, 1991) that this happened at least four times, that is, in Brachychthonioidea, Enarthronota, and twice in Nothrina. As this is unique in the animal kingdom (see Tucker et al., 2013), studying Oribatida is most promising for understanding evolutionary consequences of the loss of sex (Heethoff et al., 2007; Palmer & Norton, 1992; Schwander et al., 2014). The diversification of these taxa into different taxonomically recognized species indicates that they successfully split into morphologically coherent units without engaging in sexual processes. However, it remains to be shown whether these diversifications were adaptive or not (Gittenberger, 1991; Schluter, 2000).

Remarkably, the four species‐rich parthenogenetic clusters of Oribatida are very old and likely originated 400–300 mya in Devonian, Carboniferous, and Permian times (Schaefer & Caruso, 2019; Schaefer et al., 2010). In contrast to the commonly held view that parthenogenetic lineages are short lived, it is increasingly realized that there are a number of old asexual taxa (Neiman et al., 2009). Recent studies in Oribatida have shown that parthenogenetic lineages manage to overcome the problems of the accumulation of deleterious mutations, possibly due to strong purifying selection related to large population size (Brandt et al., 2017). The diversification of the four clusters of parthenogenetic species in Oribatida coincides with the massive global carbon burial during the Permian/Carboniferous time (Berner, 2003) providing large amounts of resources for decomposers, presumably resulting in massive population growth favoring parthenogenetic reproduction and potentially diversification of parthenogenetic species (Scheu & Drossel, 2007). Notably, the parthenogenetic lineages survived the large mass extinction events during and at the end of the Paleozoic, potentially also due to large amounts of accumulated dead organic material (Benton & Twitchett, 2003).

Many of the Oribatida taxa that underwent parthenogenetic diversifications still occur today in habitats that resemble dominant ecosystems during Carboniferous times, for example, in boreal forests (i.e., Brachychthonioidea; Maraun & Scheu, 2000), in wet temperate forests (Nothrina), in peat bogs (Nothrina, Enarthronota; Lehmitz & Maraun, 2016), and generally in wet or aquatic habitats (Nothrina) suggesting that these habitats favor parthenogenetic species (Seniczak et al., 2016). High densities of Oribatida in these habitats (up to 200,000 ind./m2; Maraun & Scheu, 2000) further support the view that ample resource availability (as indicated by high densities) favors parthenogenetic reproduction. Overall, our findings suggest that ecological factors fostered the evolution of parthenogenesis, its long‐term maintenance, and its subsequent diversification into morphologically coherent units/species.

4.4. Re‐evolution of sex

The re‐evolution of complex characters during evolution contradicts Dollo's law (Gould, 1970) stating that complex characters once lost do not re‐evolve (Collin & Miglietta, 2008). Sexual reproduction is such a complex character that presumably evolved only once very early during eukaryote evolution (Bernstein et al., 1984). Once lost its subsequent re‐evolution therefore is unlikely (Bull & Charnov, 1985). However, there are a few cases where sexual reproduction likely has re‐evolved, once in the plant genus Hieracium (Chapman et al., 2003), in ostracods (Horne, 2010), and in Oribatida in the taxon Crotoniidae/Camisiidae (Domes et al., 2007). However, there is evidence from our study that in Oribatida sex also re‐evolved twice in Enarthronota. Re‐evolution of sex in Oribatida may have been facilitated by parthenogenetic species reproducing via automixis still undergoing meiosis (Bergmann et al., 2018). The occasional production of spanandric (i.e., very rare) males (Taberly, 1987a, 1987b, 1987c) indicates that they never lost the ability to produce males.

Understanding the driving factors for the re‐evolution of sex is difficult. An interesting pattern related to the re‐evolution of sex is that the species/lineages which re‐evolved sex either are tropical but originated in temperate regions (Pachl et al., 2017) or still live in temperate regions (Crotonia brachyrostrum, Apoplophora sp., Mesoplophora cubana). Oribatida communities in the temperate or boreal zone generally include more parthenogenetic taxa than those in the tropics (Maraun et al., 2019; Pachl et al., 2017). Possibly, the more abundant parthenogenetic species/lineages in temperate and boreal habitats provided more opportunities for the transition to sex. However, the factors which drove these transitions remain enigmatic but might be related to more scarce and more patchily distributed resources (Scheu & Drossel, 2007; Song et al., 2011).

CONFLICT OF INTEREST

The authors have no conflict of interest.

AUTHOR CONTRIBUTION

Patrick Pachl: Conceptualization (equal); Data curation (equal); Formal analysis (equal); Methodology (equal); Software (equal). Matti Uusitalo: Data curation (equal); Validation (equal). Stefan Scheu: Conceptualization (equal); Formal analysis (equal); Writing‐review & editing (equal). Ina Schaefer: Conceptualization (equal); Data curation (equal); Formal analysis (equal); Investigation (equal); Software (equal); Supervision (equal); Visualization (equal); Writing‐review & editing (equal). Mark Maraun: Conceptualization (equal); Formal analysis (equal); Investigation (equal); Project administration (equal); Supervision (equal); Validation (equal); Visualization (equal); Writing‐original draft (equal); Writing‐review & editing (equal).

Supporting information

Fig S1

Click here for additional data file. (149.1KB, pdf)

ACKNOWLEDGEMENTS

We thank Roy A. Norton for collecting several Acariformes for this study, and for commenting on an earlier version of the paper. Open access funding enabled and organized by Projekt DEAL.

Pachl P, Uusitalo M, Scheu S, Schaefer I, Maraun M. Repeated convergent evolution of parthenogenesis in Acariformes (Acari). Ecol Evol.2021;11:321–337. 10.1002/ece3.7047

DATA AVAILABILITY STATEMENT

All data are published in NCBI (for GenBank accession numbers see Table 1).

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Associated Data

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Supplementary Materials

Fig S1

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Data Availability Statement

All data are published in NCBI (for GenBank accession numbers see Table 1).

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