Research Article
Research Article
Breakaway from a globular body shape: molecular phylogeny reveals the evolutionary history of the enigmatic springtail Mackenziella psocoides
expand article infoClément Schneider, Cyrille A. D’Haese§
‡ Senckenberg Gesellschaft für Naturforschung, Görlitz, Germany
§ Muséum national d’Histoire naturelle, Paris, France
Open Access


Mackenziella psocoides Hammer, 1953 (Collembola: Mackenziellidae) is a widespread but uncommon springtail. Its unusual body shape (ovoid, with partial coalescence of abdominal segments) has puzzled the specialists for a long time, until the discovery of males allowed to relate the species to a family of globular springtails, the Sminthurididae. Yet, the precise phylogenetic position of M. psocoides, and hence of the Mackenziellidae, remained ambiguous. In this work, we report a new locality for M. psocoides in Germany. We provide the first DNA sequences (nuclear ribosomal DNA operon) for the species, as well as the first images using scanning electron microscopy. We investigate its phylogenetic position based on the molecular data and specify details on its morphology. Our results show that M. psocoides is nested inside of Sminthurididae, as the sister group of Sphaeridia Linnaniemi, 1912. Consequently, Mackenziellidae syn. nov. is here synonymized with Sminthurididae. We include Mackenziella and Sphaeridia in the Sphaeridiainae subfam. nov., a replacement name for Sphaeridiinae Richard, 1968 that is a junior homonym of Sphaeridiinae Latreille, 1802 (Coleoptera: Hydrophilidae). Corresponding to its phylogenetic position within Sminthurididae, the evolutionary origin of M. psocoides is younger than previously thought (79 mya +/- 35 my). The lineage accumulated an unusual amount of body modifications involving, among others, the loss of the globular body shape. This rapid rate of evolution is, to our knowledge, unique in springtails. It shows that globular body shape is not an evolutionary dead-end, and the secondary acquisition of a linear body shape and recovery of longitudinal flexibility is still possible.

Key words

Body shape evolution, Oxford Nanopore, body segmentation, SEM, Sminthurididae, Mackenziellidae, Symphypleona, new synonym

1. Introduction

Collembola (springtails) form one of the four classes of Hexapoda and are also the most ancient undebated Hexapoda found in the fossil record (Rhynie cherts, early Devonian) (Hirst and Maulik 1926; Massoud 1967a; Greenslade and Whalley 1986). They are primitively of elongated shape, with three thoracic segments and six abdominal segments, a morphology that is conserved in the order Poduromorpha. The orders Entomobryomorpha, Symphypleona and Neelipleona are characterized by the partial reduction of the prothorax (D'Haese 2003) (volume reduction and regression of the pronotum). Symphypleona and Neelipleona underwent a drastic evolutionary trajectory leading to the acquisition of a globular body shape (Fig. 1A–C) through the fusion of at least the third thoracic to the fourth abdominal segments, with the second thoracic and fifth abdominal segments being further co-opted in this process in some lineages (Betsch 1980; Schneider 2017). In Neelipleona, the abdomen is reduced, smaller than the thorax, while in Symphypleona the abdominal region is larger than the thorax (Massoud 1976). In both orders, the head acquired a hypognathous posture.

Figure 1. 

Sampled species of Sminthurididae A Sminthurides aquaticus, B Stenacidia violacea, C Sphaeridia pumilis. Mackenziella psocoides D Male (left) and female (right) during courtship (fixed in ethanol), E juvenile, F, G, H, I female on water surface, various angles, J female (one of the largest specimens obtained), K Mackenziella psocoides (left) and a co-occurring young Sphaeridia pumilis (right).

Mackenziella psocoides Hammer, 1953 is the unique species of the family Mackenziellidae Yosii, 1961. It is also one of the smallest and strangest Collembola, being a tiny, ovoid animal with a prognathous head, and retaining a marked segmentation until the second abdominal segment (Fig. 1D–K), a prothorax devoid of dorsal chaetae and a small furca. It has puzzled the specialists for a long time and was in turn related to the families that are now classified in Poduromorpha (Hammer 1953; Hüther 1964), Neelipleona (Pactl 1956; Moen and Ellis 1984) and Symphypleona (Yosii 1961; Christiansen and Bellinger 1981). Salmon (1956) placed it in Poduridae (Poduromorpha) but estimated that it could be closer to Actaletidae (Entomobryomorpha). Massoud (1967b), followed by Christiansen and Bellinger (1981), guessing that the known specimens were juveniles. This history of early studies and opinions on M. psocoides has been reviewed in detail by Fjellberg (1989).

Fjellberg (1989) made a significant contribution to the systematics of the species by providing a detailed description based on many specimens, confirming that the species was described from adult females and describing the first males. He showed that males are equipped with the male antennal clasping organ (MACO), a modification of the antennae, allowing the male to grab the female antennae during courtship (Figs 1D, 4B, E, F). This organ is a synapomorphy of the Sminthurididae (Symphypleona). Fjellberg (1989) suggested that M. psocoides was the sister-group of Sminthurididae, with the following synapomorphies: presence of the MACO and absence of the female anal appendages (present in all the other families of Symphypleona). Fjellberg (1989) interpreted the elongate body shape and prognathous head as secondary modifications (apomorphies) of M. psocoides. Fjellberg’s (1989) views were accepted by Sánchez-García and Engel (2016a) who reused the name Sminthuridida (a synonym of Sminthurididae) as a suborder grouping Sminthurididae and Mackenziellidae. Sminthuridida is sister to the Appendiciphora (all the other Symphypleona).

Despite the complete morphological redescription provided by Fjellberg (1989), the precise systematic position of M. psocoides has remained disputable. The absence of female anal appendages can currently only be seen as a plesiomorphy in Symphypleona (Bretfeld 1999), and hence their absence does not provide any clade support. The only clear synapomorphy of M. psocoides and the Sminthurididae is the MACO. Indeed, M. psocoides possesses the simple version of the MACO, almost identical to the one found in Sphaeridia Linnaniemi, 1912 (Massoud and Betsch 1972, Fjellberg 1989). From a strict parsimony point of view, this is counterweighted by the secondary acquisition of an elongated body shape and of the regression of the furcal segment (always well developed in Symphypleona). An alternative scenario from the Sminthuridida sensu Sánchez-García and Engel (2016a) hypothesis would be the sister relationship of Symphypleona and Mackenziellidae, involving a common ancestor characterized by an elongated body shape and a MACO, and the subsequent acquisition of globular shape in Symphypleona and the loss of the MACO in the Appendiciphora.

Could a globular springtail have made a U-turn on its overall body shape evolution and regain the elongated body shape? Answering this question requires to resolve the precise phylogenetic placement of M. psocoides. However, M. psocoides is a rare species that has never been sequenced so far (da Silva Medeiros et al. 2022). The absence of molecular data for M. psocoides was mentioned and regretted in recent phylogenetic works dealing with higher taxa of Collembola (Sun et al. 2020; Bellini et al. 2022) as well as in the recent review on Sminthurididae systematics by da Silva Medeiros et al. (2022).

We discovered a new locality for M. psocoides, in Saxony (Germany), that yielded over a hundred of specimens, allowing us to fill this gap and further study the species. In this work, we conducted a morphological investigation with light microscopy for comparison with the population described by Fjellberg (1989), examined the ultrastructure of the tegument and of the external organs using scanning electron microscopy (SEM), and revealed the phylogenetic position of M. psocoides within Collembola using the complete nuclear ribosomal DNA operon, with improved sampling in the Sminthurididae. The ecological, evolutionary, and systematic implications of our findings are discussed.

2. Methods

Sampling. The first sample of mosses growing on a concrete slab (Fig. 2A–C) was hand-collected on 12th February 2023 stored in a bag for 5 days at room temperature, then put on a Berlese (sample A). After 48 hours, Mackenziella specimens were noticed in the collection tube (99% ethanol). On 18th February 2023, the locality was visited again, the same habitat was sampled again twice: sample B and C, a few meters apart from each other, and each roughly twice the size of sample A. Additional samples were taken in the area, targeting similar mosses but growing directly on soil.

Figure 2. 

Habitat of the population of M. psocoides studied in this work, A context, B, C close-up.

Macrophotography. Specimens from the second sampling were collected alive in a tube containing a moistened chunk of the original habitat. Macrophotographs of living individuals were taken using a Fujifilm X-T3, either with a Laowa Ultra-Macro 2.5-5X objective at f5.6 and 5× magnification, or mounted on a Leica S8AP0 stereomicroscope, at full magnification.

Light microscopy. Fifteen specimens (11 females, 4 males) were cleared in lactic acid and mounted on microscope slides in Marc-André II medium. Observations were done with a compound microscope with phase contrast, up to 100× magnification.

Scanning Electron Microscopy (SEM). Five specimens (2 females, 3 males) were transferred in 100% ethanol, critical point dried with a Leica EM CPD300 and platinum coated to a thickness of 7.13 nm with a Leica ACE600. Observations were carried out with a Hitachi SU3500 scanning electron microscope using 15 kV accelerating voltage and backscattered electron (BSE) for image magnifications ranging from 450× to 30,000×.

DNA sequencing. Genomic DNA (gDNA) was individually extracted from four specimens and an additional gDNA extract was made from a pool of five specimens, all using a modified protocol for the Qiagen MagAttract HMW extraction kit (Schneider et al. 2021). We also newly sequenced individuals of Stenacidia violacea (Reuter, 1881) and Sminthurinus elegans (Fitch, 1862) to improve the sampling of Sminthurididae and Katiannidae (Symphypleona). The ~6.4kb long nuclear rDNA operon was amplified with a single PCR, using primers newly designed (as part of a parallel work that will be separately presented) and the long range and high fidelity Q5® polymerase HotStart master mix (NEB). Forward primer: 5’-CTCAAAGATTAAGCCATGCATGTC-3’, reverse: 5’-RAGTCTCAACGGATCGCAGC-3’. Amplification was done following NEB standard recommendations for the Q5 and using an annealing temperature of 65°C (computed using NEB Tm Calculator).

Two specimens, plus the pool, were amplified successfully. The amplicons were purified using the Qiagen MagAttract HMW kit purification steps and resuspending the purified DNA in water. The amount of purified DNA was measured with a Quantus fluorometer (Promega) using the dsDNA assay kit. Libraries were prepared using the Nanopore Rapid Barcoding Kit 96 (SQK-RBK110-96). Amplicons were normalized to 50 ng prior to the tagmentation step and then pooled. Library preparation followed the standard protocol (protocol version RBK_9126_v110_revD_24Mar2021). The pooled library was sequenced on a Nanopore MinION using a Flongle flow cell (R9.4.1), and MinKNOW configured to run Fast basecalling. For each sequenced library, 1500 of the longest reads were selected and mapped to a reference sequence (Folsomia candida) using Geneious. A majority consensus was called after visual inspection and trimmed to the primer binding sites (excluded). The consensus was further polished by mapping 3000 of the longest reads on it.

Phylogenetic reconstruction. We used 18 collembolan species covering the four orders (Fig. 8, Genbank accession numbers provided in Table 1), for which the full-length nuclear rDNA was available. Fifteen sequences were obtained from third party projects. Sequences of Desoria tigrina Nicolet, 1842, Folsomia candida (Willem, 1902), Orchesella cincta (Linnaeus, 1758), Sinella curviseta (Brook, 1882) and Sminthurides aquaticus (Bourlet, 1842) were retrieved from publicly available genomes (Faddeeva-Vakhrusheva et al. 2016, 2017, Zhang et al. 2019, Schneider et al. 2021). The other nuclear rDNA sequences were obtained from, yet unpublished, PacBio based genome assemblies (Schneider et al. in prep.) and Illumina sequencing based genomes assemblies (Collins et al. 2023 preprint). Whole genomes will be released in a separate work. The sequences were aligned using MUSCLE (v3.8.31). Since one of the available species was missing the ITS1, 5.8S rDNA and ITS2 (not assembled), we removed those regions from the alignment. The phylogeny was inferred under Maximum Likelihood criterion using IQ-TREE (v2.1.3; Minh et al. 2020), with automatic model test and selection (-m MFP), node support was assessed using nonparametric bootstrap using 100 replicates (-b 100) and SH-aLRT (-alrt 1000).

Table 1.

List of species included in the phylogenetic analysis, with Genbank accession number. *Accession to genome assembly (or biosample when assembly is yet unavailable), the extracted 18S and 28S rDNA sequences can be directly retrieved from the Zenodo data archive (

Order Family Species Genbank accession number Data provider
Entomobryomorpha Entomobryidae Lepidocyrtus violaceus OR149202 Schneider et al. in prep.
Entomobryomorpha Entomobryidae Sinella curviseta GCA_004115045* Zhang et al. (2019)
Entomobryomorpha Isotomidae Desoria tigrina GCA_906901685* Schneider et al. (2021)
Entomobryomorpha Isotomidae Entomobrya marginata OR149203 Schneider et al. in prep.
Entomobryomorpha Isotomidae Folsomia candida GCA_002217175* Faddeeva-Vakhrusheva et al. (2017)
Entomobryomorpha Isotomidae Folsomides angularis OR149205 Schneider et al. in prep.
Entomobryomorpha Orchesellidae Orchesella cincta GCA_001718145* Faddeeva-Vakhrusheva et al. (2016)
Neelipleona Neelidae Megalothorax cf. minimus OR149198 Schneider et al. in prep.
Neelipleona Neelidae Neelides folsomi SAMN25040855* Collins et al. (2023) [preprint]
Neelipleona Neelidae Neelus murinus SAMN25040856* Collins et al. (2023) [preprint]
Poduromorpha Poduridae Podura aquatica OR149201 Schneider et al. in prep.
Poduromorpha Tullbergiidae Paratullbergia callipygos SAMN25040870* Collins et al. (2023) [preprint]
Symphypleona Katiannidae Sminthurinus elegans OR149196 This work
Symphypleona Sminthuridae Sminthurus viridis OR149204 Schneider et al. in prep.
Symphypleona Sminthurididae Mackenziella psocoides OR149199 This work
Symphypleona Sminthurididae Sminthurides aquaticus GCA_906901655* Schneider et al. (2021)
Symphypleona Sminthurididae Sphaeridia pumilis OR149200 Schneider et al. in prep.
Symphypleona Sminthurididae Stenacidia violacea OR149197 This work

Time calibration. The same molecular data set was used to estimate the time of divergence of Mackenziella. The fossil record of Collembola is very scarce. Calibration was carried out using the most ancient known representant of a given group to provide an estimate of the age. The root age of Collembola is based on Rhyniella praecursor (at least 420 Mya); the age of Poduromorpha, Isotomidae, Entomobryidae and Sminthurididae are based on Protodontella minicornis Christiansen & Nascimbene 2006, Proisotoma communis Sánchez-García & Engel 2016b, Entomobrya pilosa Koch & Berendt 1854 and Pseudosminthurides stoechus Sánchez-García & Engel 2016a respectively. These were chosen from the exhaustive commented list of Collembola fossils by Sánchez-García and Engel (2016a, b) for an exhaustive and commented list of Collembola fossils, and the ages of amber inclusions were updated according to Seyfullah (2018). Divergence times were inferred using BEAST2 v.2.7.3 (Bouckaert et al. 2019), substitution models of all partitions were calculated using bModelTest package, calibrations were carried out with a relaxed lognormal molecular clock with an offset to the given group equal to the oldest estimated age of the fossil belonging to that group. Two independent runs of 150 106 generations were done. The first 22 % of the sampled trees were discarded as burn-in on checking likelihood trace plot, the tree files were then combined with LogCombiner and finally the resulting trees were summarized in a Maximum Clade Credibility with TreeAnnotator.

Ancestral character states reconstruction. The character states of the last common ancestor of M. psocoides and its closest found relative are inferred through direct optimization using an unweighted parsimony criterion (for discrete characters). Continuous ancestral character states (female maximal body size) are estimated with the function ace from the R package PHYTOOLS, using the Maximum Clade Credibility tree as input, and setting the method to ‘REML’ (Restricted Maximum Likelihood) and model to ‘BM’ (Brownian Motion). Maximal body sizes were directly observed or collected from literature (Fjellberg 1998a; Bretfeld 1999; Potapov 2001; Dunger and Schlitt 2011; Jordana 2012; Schneider 2017). The matrix of discrete morphological characters for Symphypleona is provided in Table S1, the body size of all sampled species is provided in Table S2. The complete analysis folder of the ancestral body size estimation is deposited on Zenodo (

Notes on species nomenclature. The taxonomic status of worldwide populations of M. psocoides is arguably ambiguous, as only the specimens from Canary Islands examined by Fjellberg (1989) are described with complete chaetotaxy details. The South African populations were referred as M. cf. psocoides (Liu et al. 2012). In this work we refer to M. psocoides as a single species (see Discussion). We decided to not abbreviate the genera names Sphaeridia, Sminthurides and Stenacidia in species names, to avoid confusion.

Morphological nomenclature. Nomenclature of the eye follows Guthrie (1906), nomenclature of the labial palp follows Fjellberg (1998b), nomenclature of male antennal article II and III after Massoud and Betsch (1972) and Fjellberg (1989). Abbreviations used: Abd. – Abdominal segment, Ant. – antennal article, MACO – male antennal clasping organ, Th. – Thoracic segment.

3. Results

3.1. Ecology

Mackenziella psocoides was found in the shallow mattress of mosses (dominant Brachythecium albicans and intermixed Ceratodon purpureus) growing on a path of concrete slabs in a peri-urban context (Fig. 2A–C). The path is enclosed between a road and a concrete sidewalk, with only a thin border of ground covered with herbs. The mosses were sampled with its substrate, being a 1–2 cm deep layer of organic matter and soil particles mixed with coarse sand and small gravels. At the time of collection, the sample was humid, but unfrozen (sampling occurred 24 hours after the last frost event). The second collection occurred after one week of cold temperatures (two nights near 0°C, and up to 10°C), without precipitation. The day of collection itself was rainy and the new samples were well-moistened.

Mackenziella psocoides was very abundant in sample A (> 100 specimens), and in low abundances in sample B (4 specimens) and C (~ 30 specimens) (B and C each being roughly twice the size as sample A in terms of moss sampled). Even in sample A, M. psocoides was evidently the smallest contribution to the overall collembolan biomass.

Hypogastrura vernalis (Carl, 1901) was dominant in terms of relative abundance and biomass in all three samples. Hemisotoma thermophila (Axelson 1900) was rather common in all samples. Folsomides angularis (Axelson, 1905) was common in sample B but absent from A and C. Sminthurididae sp. (likely Sminthurides sp., only juveniles found, whitish, each with the tibiotarsal III organ) was rather common in sample A, and almost absent from sample B and C. Sminthurinus cf. elegans was found in low numbers in all samples. Sphaeridia pumilis (Krausbauer, 1898) was found only in sample C, in roughly the same numbers as M. psocoides. Lepidocyrtus lanuginosus (Gmelin 1790), Orchesella cincta (Linnaeus, 1758) and Agrenia sp. were found in moderate abundance (but high biomass) in sample A and C, but not B.

3.2. Morphological examination

Mackenziella psocoides Hammer, 1953

Material examined for morphology

Eight females and three males on eleven slides; Germany, Saxony, Tauchritz near Görlitz; 51.0689°N, 14.9340°E, alt. 210 m; 12 Feb. 2023; C. Schneider leg.; mosses and shallow substrate on a concrete slab; extracted with Berlese funnel; deposited in the Apterygota collection of the Senckenberg Museum für Naturkunde Görlitz; slides number AA00001 to AA00011. Three females and a male on four slides; two females and three males on a SEM mount plate; same data as above; deposited in the Apterygota collection of the Muséum National d’Histoire Naturelle, Paris; slides number EA060065, EA060066, EA062721 and EA062722, SEM plate number EA030050.

Additional description

Our specimens are very similar to the descriptions of Fjellberg (1989, 1998b, 2007), which we do not intend to fully repeat here. Nonetheless, we report a few additional observations and precisions.

Habitus as in Figs 1D–K, 3A–E

Male with a higher ratio length head/trunk than female (Fig. 3A–D). Clypeal area reduced (Figs 3E, 5A). Dorsally on head, with a deep transverse groove posterior to the eyes (Fig. 3A, C, D). With a dorsal bulge b at the head-Th. I insertion (Fig. 3A, D). With four dorsal bulges corresponding to Th. II–Abd. III, well-marked in either living, ethanol preserved and dried specimens (Figs 1D–J, 3A, C, D), but almost erased in lactic-acid induced swollen specimens. Abd. I and II bulges well-marked in male, but faint in female (Fig. 3A, C, D). Abd. IV delimited from Abd. V by a faint groove (Fig. 3A, C, D). Dorsally, Abd. III + IV region twice as long as Abd. I + II. Ventrally, retinaculum (Abd. III appendage) at mid-distance between the ventral tube (Abd. I) and the furca (Abd. IV appendage). Furca short, barely reaching the posterior side of the ventral tube when folded.

Figure 3. 

Mackenziella psocoides habitus SEM microphotographs. A dorsal view, female, B ventral view, female, C dorsal view, male, D lateral view, male, E frontal view, male. Abbreviations: b – head-Th. I bulge, t – integumental tubercle, s – sensillae in a depression on a papilla. Scale bars: 50 µm.


Integumentary secondary granules resulting from simple and individual outgrown primary granules (increased in size and elevated above the ordinary primary grain) (Fig. 6E). Presence limited to: postantennal area dorsally to the eyes (Fig. 5A, B), head–Th. I dorsal bulge, dorsal and lateral part of Th. II–Abd. V (Figs 3A, C, D, 6A). Absent from clypeal area and mouth part (Fig. 5A) and from all appendages. Dorso-median line of Th. II–Abd. III not marked, but terminal tubercle t present as a roundish prominence without secondary granules (Figs 3A, 6E). Linea ventralis straight, without additional integumentary channels (Fig. 4A), associated with three pairs of tubercles (Fig. 4A). Males without vesicles on Th. III.

Figure 4. 

Mackenziella psocoides. A Linea ventralis, arrows indicate the ventral tubercles, B male ant. II and III (clasping organ), posterior side. Antennae SEM microphotographs. C right antenna dorsal view, female, D tip of antennal segment IV, female, E left antenna fronto-ventral view, male, F right antenna dorsal view, male. Abbreviations: B1 – chaeta b1, C3 – chaeta c3, m – microelement setiform, ms – microelement spine-like, p – Ant. III organ deep lateral pit, s – Ant. III organ sensillum (one very small, one larger), S – Ant. III large s-chaetae with rounded apex.

Figure 5. 

Mackenziella psocoides SEM microphotographs. A head frontal view, male, B eyes, A, B, C, E, F, G, H – ocelli, Oc – ocular chaeta, C mouth, A, B, C, D, E – labial palp apical papillae, a1, b2, b4, d1, d2, d4, e – labial palp guard chaetae, e – labial palp guard chaetae. D ventral tube.

Figure 6. 

Mackenziella psocoides SEM microphotographs. A Abdominal segment V and VI (anal valves), female, B tibiotarsus I ventral view, C tibiotarsus II dorso-lateral view, D tibiotarsus III ventral view, E Abd. III middorsal tubercle with first pair of axial chaetae, F Abd. II sensillum in a depression on a papilla, male. Abbreviations: s – sensillae, ae, ai, e, i, ja, jp, pe, pi – tibiotarsus chaetae, I, II, IV – tibiotarsus chaetae row.


Chaetae smooth, without ornamentation (Fig. 4B–F). Most of the long chaetae of Ant. IV with a rounded apex (Fig. 4C–E). Male also with two long s-chaetae with rounded apex on Ant. III and three on Ant. II (Fig. 4B, E, F); ms on Ant. III as a microchaetae (Fig. 4B, F) (otherwise as described in Fjellberg 1989).


Mouth as in Fig. 5C, without oral fold nor maxillary outer lobe. Labrum and labium as described in Fjellberg (1989, 1998b).


Tibiotarsus I apical row with chaeta ja flattened with an external groove, and apressed to the tegument (not erected), on ventral side (Fig. 6B). Unguis with a dorsal smooth lamella splitted in two basally, the two anterior and posterior halves each joining with a small pseudonichya, the dorsal, basal side of the claw forming a depression covered with primary grain (Fig. 6C). Unguiculus I to III respectively with: apical filament, short apical filament, no apical filament (Fig. 6B–D); unguiculus tri-lamelate, each lamella with a smooth ridge (Fig. 6B–D).


Posterior part of dens with up to four chaetae ornamented with spicules (discovered with SEM, apparently smooth in some specimens) (Fig. 7B–D). Mucro either separate or fused to the dens (as reported in Fjellberg 1989 for juveniles), but fused form may be found in apparently mature specimens. Mucro posteriorly without lamellae, anteriorly, with a smooth lamella, either with an inner groove (separate mucro form) or not (fused mucro form). This smooth lamella extending to the apex of the mucro and shaping its rounded tip.

Figure 7. 

Mackenziella psocoides furca SEM microphotographs. A furca anterior side, female; detail: chaetae on lateral side on base of furca, B furca anterior side, female, C furca posterior side, female, D furca posterior side, male, E retinaculum.

Other ventral organs

Sternite of Abd. IV with a pair of small chaetae (Fig. 7A) not mentioned in Fjellberg (1989). This pair of chaetae sometimes missing or incomplete (only on one side). Probably homologous to the ventral-anterior field of chaetae found on Abd. IV of most Symphypleona. Ventral tube of the male simple (Fig. 5D). Retinaculum simple, with 3+3 teeth and no basal tubercle (Fig. 7E).

3.3. Sequencing and Phylogeny

The three sequenced libraries for M. psocoides resulted in three identical sequences. Thus, a single sequence was used to represent the species in the phylogenetic tree. The recovered tree (Fig. 8) was compatible with the monophyly of all orders. Mackenziella psocoides was found to be the sister group of Sphaeridia pumilis, this node being the sister of another clade formed by Sminthurides aquaticus and Stenacidia violacea, all supported with high bootstrap support (>=99%) in the ML tree and with maximum posterior probability (1) in the Bayesian analyses. In the rest of the text, we refer to Sminthurididae as a monophyletic group, including M. psocoides. Within Symphypleona, the relations were as such: (Katiannidae, (Sminthuridae, Sminthurididae)) with a moderate support to the basal node (bootstrap = 84.4%).

Figure 8. 

Maximum clade credibility tree based on the trimmed alignment of the combined 18S rDNA and 28S rDNA. Node support values: posterior probability/nonparametric bootstrap (100 replicates)/aLRT (1000 replicates); blue bars indicate 95% HPD intervals of the age estimates, age estimate in red above the branches. Nodes with less than 75% bootstrap or 0.7 posterior probability support are collapsed. Habitus of Sphaeridia pumilis and M. psocoides represented next to the corresponding labels (M. psocoides drawing modified after Fjellberg 1989).

The mean crown age for Mackenziella + Sphaeridia was estimated at ~79 Ma (42–113 Ma). The crown age of Sminthurides + Stenacidia was estimated at 68.79 Ma (31–106), the crown age of Sminthurididae at ~126 Ma (113–158). The origin of the four Collembola orders seems to be rooted in the Paleozoic (or possibly Mesozoic considering the lower part of the range), with mean crown age of ~261 (169–363) Ma, ~285 (194–398) Ma, ~159 (100–309) Ma and ~336 (211–427) Ma for Entomobryomorpha, Symphypleona, Poduromorpha and Neelipleona respectively. These results have to be taken with caution, considering the restricted taxon sampling used in our analyses and, more importantly, the known collembolan fossil record being very scarce. The ML and Bayesian trees are independently shown in Fig. S1 and Fig. S2. The complete analysis folder is deposited on Zenodo (

3.4. Ancestral character states reconstruction

No evident morphological synapomorphies of Sphaeridia + Mackenziella could be found. Direct optimization of character states at the (Sphaeridia, Mackenziella) node results in: globular body shape, orthognathous head, simple MACO, mouth parts present, slender antennae, large clypeal area, complete mouth parts, eyes with eight ocelli, prothorax without prominent bulge, absence of vesicles on metathorax (male), long furca at least reaching the prothorax segment when folded under the body, long mucro with a pair of posterior lamellae, retinaculum with presence of chaetae (adult) and basal tubercles, five pairs of abdominal trichobothria, absence of Tibiotarsus III organ. Those ancestral character states are all unchanged in the genus Sphaeridia, and also apply to the Sminthurididae ancestor (but state of MACO arguably ambiguous). The ancestral body size estimation indicates a reduction of the size in branch leading to Sphaeridia and Mackenziella (with an ancestor estimated around 650 µm, against 910 µm for the ancestor of Sminthurididae). The tree annotated with all estimated ancestral body sizes is provided in Fig. S3.

4. Discussion

4.1. Species distribution

Mackenziella psocoides is reported from North America (Hammer 1953), Scandinavia (Fjellberg 1988, 2007), Western and Central Europe (Hüther 1961, Pomorski 2000, Berg 2018, this paper), North Africa (Fjellberg 1989) and South Africa (Liu et al. 2012). Known localities are indicated in Fig. 9 and Table S3. Despite this wide distribution range, the species is uncommonly found. Of the two dozen reported findings, only Fjellberg (1989) found it in very large abundance (about 150 specimen), in the Canary Islands (Tenerife, La Palma and La Gomera). Another population of Mackenziella is regularly found in the region of Cape Town, South Africa (Liu et al. 2012 and C. Janion-Sheepers pers. comm.), where it is assumed to be invasive (Liu et al. 2012). Our specimens could not be distinguished from the description by Fjellberg (1989) based on specimens from the Canary Islands. Given that Fjellberg (1988, 2007) also recognized the same species in Scandinavia, we assume that the European and North African populations belong to the same morphological species. Hammer (1953) original description based on two specimens from Canada, indicated 4+4 teeth on the retinaculum (instead of 3+3 as in our specimens). Fjellberg (1989) examined the type specimens but could not distinguish the actual state of their retinaculum. Novel collection in the Nearctic and in the Southern Hemisphere will be necessary to confirm the morphological homogeneity of M. psocoides populations worldwide. Since some collembolan species are known to hide a large molecular diversity behind homogeneous morphology (e.g., Schneider and D'Haese 2013, von Saltzwedel et al. 2017), further genetic investigations are also desirable.

Figure 9. 

Reported findings of M. psocoides. Marker: blue – type locality, yellow – this work new locality, green – previous records.

4.2. Species ecology

Mackenziella psocoides is related to poor habitats exposed to drought: moss and vegetation on sand and rocks, sandy meadow (Berg 2018). In the Canary Islands, it was found on wind swept open ridges in the forested zone with sparse moss cover on the ground (A. Fjellberg, pers. comm.). It was found in proximity to a coal mining site near Spremberg in Germany (D. Russel, pers. comm.): we sampled this locality in November 2022 but could not find it there. The population sampled by us for this paper was apparently restricted to the concrete slabs path; similar mosses sampled around, but growing directly on the ground, did not yield it. In summer, the shallow substrate on the slabs is likely to dry out, without any options for the individuals to escape in the depth. Fjellberg (1989, 2007) suggested M. psocoides to be adapted to dry habitat through drought resistant eggs.Berg (2018) reached the same conclusions by reviewing all the findings of M. psocoides so far, indicating a preference for nutrient-poor, exposed habitats with shallow vegetations. This trait could also have allowed M. psocoides to reach a cosmopolitan distribution through airborne dispersal of the eggs (Fjellberg 1989). Our sampling shows the ability of M. psocoides to reach and colonize a small island of suitable habitat.

M. psocoides seems also to have a winter affinity. It was active shortly after the defrosting of its habitat. The defrosting may have triggered a rapid bloom of the population from diapause eggs, which was then already in decline one week later. However, fine observations would be needed to ascertain this. It is unclear if the individuals themself can withstand drought or frost through mechanisms of anhydrobiosis or cryoprotective dehydration known in several springtail species (Holmsrtrup 2018 and references therein).

Among the springtails found in the same habitat, we find notable the presence of F. angularis and Sphaeridia pumilis, both widespread and common species. Folsomides angularis is an indicator of dry habitats, well known for coping with drought through anhydrobiosis (Belgnaoui and Barra 1989). In Europe, it is commonly found in low-growing vegetation on exposed rocks (Fjellberg 2007), and it can settle in extreme environments such as the Namib desert gravel plains (Collins et al. 2019). Sphaeridia are the closest relatives of M. psocoides. Sphaeridia pumilis and M. psocoides were found together in one of the samples. This proximity was also observed by Fjelberg (1989) in the Canary Islands, who extracted a few individuals of M. psocoides from Euphorbia balsamifera litter and sand samples (collected dry, wetted before Berlese extractions), among several hundreds of Sphaeridia pumilis and Folsomides species (dominant F. terrus Fjellberg, 1992) (Fjellberg, comm. pers.). While we did not find any further mention of specific drought resistance for Sphaeridia pumilis, drought resistant eggs have been reported in Sphaeridia (Greenslade 1981). This trait could be ancestral to Mackenziella + Sphaeridia lineage. However, Sphaeridia does not only contain xerophilous species: the species from the tropical cloud forest of Ecuador (Bretfeld and Trinklein 2000) are likely never exposed to drought. The reduction of the mouthparts in Mackenziella (compared to the well-developed chewing-type mandibula in Sphaeridia) and its rarity suggest some specialization in food resources and micro-environmental conditions, while the co-occurring Sphaeridia pumilis may be more generalist.

We found M. psocoides, F. angularis and Sphaeridia pumilis in the same habitat, but with low overlap in the three distinct samples, hinting at a possible space or time exclusion of the species at fine scale. Further sampling is required to understand the dynamic of the springtail community in exposed habitats.

4.3. Phylogeny

Our phylogenetic inference based on the nuclear rDNA, not only confirms Fjelberg (1989) views that Mackenziella is related to Sminthurididae but reveals that M. psocoides is a member of Sminthurididae, actually a close relative to Sphaeridia. The precise phylogenetic positioning of Mackenziella allows to draw its singular evolutionary history, as a member of Sminthurididae that reverted to an elongated body shape. The present phylogeny also indicates the paraphyly of Appendiciphora, with two possible evolutionary scenarios:

(1) the independent acquisition of the female anal appendages: once in Katiannidae (and presumably Arrhopalitidae not sampled here), and once in Sminthuridae (and presumably Bourletiellidae and Dicyrtomidae not sampled here)

(2) loss of those appendages in Sminthurididae.

The bootstrap support remained weak and we do not aim to further address this question here.

4.4. Comparative morphology

Eye. In most Sminthurididae, the eye is composed of eight ocelli (labeled A to H after Guthrie 1906). The ocelli C and D are usually reduced, e.g., in Sminthurides aquaticus and Sphaeridia pumilis (Fig. 10A, B). In species reported with reduced eyes such as Sminthurides sexoculatus Betsch and Massoud, 1970, C and D are missing. Palacios-Vargas et al. (2018) mislabelled the ocelli in the eye of Denisiella betschi Palacios-Vargas et al., 2018 and Denisiella rhizophorae Palacios-Vargas et al., 2018, and the small ocelli C and D have been overlooked (reduced, but still visible on their figs 12A and 25, in a similar configuration than in Sminthurides and Sphaeridia).

Figure 10. 

Left eye SEM microphotographs in frontal view. A Sminthurides aquaticus, B Sphaeridia pumilis. Arrow points in the anterior direction.

The reduction of the eye in M. psocoides can be described as follows: enlargement of C, loss of D, loss of either A or G (Fig. 5B). In Mackenziella a single chaeta is found between H and G, compared to two chaetae in the other genera of Sminthurididae (Figs 5B, 10A) (state unknown in Sminthuridia Massoud and Betsch, 1972).

Male antennal clasping organ (MACO). The four represented genera of Sminthurididae in our dataset form two clades: one including species with larger body size and complex MACO (Sminthurides + Stenacidia) and one with smaller species with simple male antennal clasping organ (Sphaeridia + Mackenziella). Following a parsimony criterion, one would assume the simple MACO to be the ancestral trait of Sminthurididae. Indeed, all Sminthurididae possess the modified chaetae of the simple clasping organ (Massoud and Betsch 1972, refer also to fig. 1 in da Silva Medeiros 2022). Those are, on Ant. II: a large chaeta (b1) on a tubercle, at least one additional smaller chaetal element (two elements only in Sminthuridia Massoud and Betsch, 1972) being small spines in the simple organ version. On Ant III, the simplest form seems limited to the large chaeta c3, in Sminthuridia. In Sphaeridia and Sminthuridia, the modified macrochaetae, possibly homologous to b2 and b3 (Ant. II), were initially not named in the antennal nomenclature of the Sminthurididae (Bestch and Massoud 1970, Massoud and Betsch 1972). Massoud and Betsch (1972) noted the variability of their presence in Sphaeridia (from 0 to 2), based on the original species description of the time, and represented a MACO devoid of additional chaetal element as the simplest form found in Sphaeridia (their fig. 9). da Silva Medeiros et al. (2022) followed this view, but associated the microchaetae of Sminthuridia to b2 and b3. At least several species of Sphaeridia possess two microchaetae in the same region.

The presence of b2 and b3 is possibly a plesiomorphy in Sminthurididae, with subsequent loss in M. psocoides and some species of Sphaeridia. However, a detailed re-analysis of Sphaeridia and Sminthuridia morphology and their internal phylogeny are necessary to gain a fine understanding of the homologies and evolution of the MACO. On the other hand, the complex MACO involves a large number of shared sub-organs following a similar organization. Those organs are on Ant. II: at least a trichobothria (Tra1) and from one to three additional modified chaetal elements (b4, b5, b6) generally mounted on a tubercle. On Ant. III from one to two additional modified chaetal elements (c1 and c2), and additional unnamed small spines and processes (variable among the genera).

Suprageneric subdivisions of the Sminthurididae based on the MACO were once suggested by Richard (1968) (in its restricted extent at the time and under the name Sminthuridinae): the Sminthuridini Börner, 1906 grouped the genera with a complex MACO and the Sphaeridiini Richard, 1968 accommodated Sphaeridia, the only genus with simple MACO at the time (also known now is Sminthuridia). However, those subdivisions were rejected by Betsch 1980 and not followed by any subsequent authors.

Claws. We note that the structure of the claws of M. psocoides is not perfectly matching the general description provided by Betsch (1980) for Symphypleona, stating “the external surface of the claw is convex and always without tegumentary grain” (translated from French). In M. psocoides, this is true in the apical part of the claw. On the basal part, the external smooth surface covers only the anterior and posterior edges of the claw, where it joins the weakly developed pseudonychia (Fig. 6C). We observed a similar condition in Sphaeridia pumilis, and Sminthurides aquaticus (for the last species, it is ascertained in claw II and III, but unclear in the fine and elongated claw I). The trait is difficult to assess with light microscopy. Claw II of Denisiella rhizophorae, also fine and long, is almost fully smooth (Palacios-vargas et al. 2018, their Fig. 12F). Further analyses are needed to understand the evolution of the claws in Symphypleona.

Tibiotarsus I. The modification of the ventro-apical chaeta ja we reported in M. psocoides is also apparent in Sphaeridia pumilis. After verification, we recognized that this chaeta was generally modified in Symphypleona (seen in representatives of Sminthurididae, Katiannidae, Sminthuridae, Arrhopalitidae, Dicyrtomidae and Bourletiellidae), a fact that is overlooked in the major syntheses on this order (Richard 1968, Betsch 1980, Bretfeld 1999).

Ventral abdominal chaetotaxy. The reduction or total loss of the ventral, anterior group of chaetae on Abd. IV may be the result of a common neotenic evolution of Mackenziella and Sphaeridia.

4.5. Systematic conclusions

From a morphological point of view, the grouping of Mackenziella and Sphaeridia lacks clear synapomorphies. The simple MACO does not have specific innovations that would be missing in the lineages with the complex MACO and may be interpreted as the plesiomorphic state within Sminthurididae. However, the nuclear rDNA operon brings a strong support to the clade.

We expect the Sminthuridini (Börner, 1906) to be a natural group, including the 10 genera of Sminthurididae with a complex MACO (da Silva Medeiros et al. 2022). The Sphaeridiini Richard, 1968 may de facto be used to regroup Sphaeridia and Mackenziella. However, Frans Janssens drew our attention to the homonymy of Sphaeridiini Richard, 1968 with Sphaeridiini Latreille, 1802 (Coleoptera: Hydrophilidae). We propose the replacement name Sphaeridiaini (type-genus: Sphaeridia Linnaniemi, 1912) formed on the entire generic name as the stem, as per recommendation 29A of the Zoological Code of Nomenclature. To adjust to the current taxonomic levels in use in Collembola higher taxa (Bellini et al. 2022), we suggest to raise those taxa to the subfamily level (Sminthuridinae and Sphaeridiainae). Mackenziellidae is a junior synonym of Sminthurididae.

We consider the position of Sminthuridia to remain unclear. Sminthuridia possesses the tibiotarsal III organ, an apomorphic character also present in most of the (above defined) Sminthuridinae, but absent in Sphaeridia and Mackenziella. Betsch (1980) used the presence-absence of the tibiotarsal III organ for the first split of its determination key of the Sminthurididae, and also represented this split in his “phyletic scheme” of the Symphypleona, while stating that the character was not informative for the family evolution. The presence of the tibiotarsal III organ but absence of a complex MACO suggests a sister relationship between Sminthuridia and the Sminthuridinae.

4.6. Mackenziella psocoides evolution

Our phylogenetic reconstruction (Fig. 8) indicates that the common ancestor of Sphaeridia and Mackenziella was a roundish Sminthurididae, bearing traits similar to modern Sphaeridia species. The ancestral body size estimation indicates that the ancestor of Sphaeridia and Mackenziella underwent some size reduction. Of course, our sampling is limited and do not allow for a precise inference of ancestral body size. Sphaeridia pumilis (0.5 mm) is among the largest species of the genus (minimal 0.3 mm observed in Sphaeridia furcata Dunger & Bretfeld, 1989). Most species from the other genera of Sminthurididae have a body size ≥ 0.5 mm (0.7 mm for Stenacidia violacea and 1 mm for Sminthurides aquaticus), smaller species being exceptional (e.g., 0.35 mm for Sminthurides monnnioti Massoud & Betsch, 1966). Since our sampled Sminthurididae species are in the upper size range of their respective genus, increased sampling would likely result in inferior or equal body size estimation for the ancestor of Sphaeridia and Mackenziella.

The transformation process from a Sphaeridia-like ancestor toward M. psocoides can be described as follows:

(1) Shortening and bulkening of the antennae

(2) Reduction of the clypeal area

(3) Reduction of the maxilla and loss of the oral fold, the maxillary outer lobe and of the mandibula.

(4) Straightening of the head from an orthognathic to a more prognathic position.

(5) Reduction of the eye.

(6) Stretching of the trunk from a globular shape toward an elongated shape (including increased distance between the retinaculum and the ventral tube). The trunk deflation emphasizes the dorsal bulges aligned with the chaetal pattern, well-marked until Abd. II. The bulges are more or less marked in other Sminthurididae (Fig. 1A–C).

(7) Formation of a granulated bulge (b) that could be interpreted as the reformation of a pronotum (or analogous structure). Alternatively, it could originate from the head occiput, pushed back dorsally during the head returns to horizontal position.

(8) Reduction of the furca from the long one reaching the first thoracic segment, toward a short one barely the ventral tube (when folded under the body).

(9) Modification of the long mucro with a pair of posterior lamellae, typical for Symphypleona and Neelipleona (Bretfeld 1986, 1999, Schneider 2017), into a short mucro with an anterior hardened ridge.

(10) Loss of chaetae and basal tubercles on the retinaculum.

(11) Loss of three of the five pairs of abdominal trichobothria (one of those remaining pairs being further reduced to small s-chaetae in the female). As suggested by Fjellberg (1989), the strongly reduced chaetotaxy of Th. II tergite is inherited from its globular ancestor.

The shortening of the antennae and the reduction of the mass of the abdomen may be the result of a neotenic process, since those traits are also observed in juveniles of Symphypleona (Fig. 1K). Assuming a “Sphaeridia-like” ancestor, we can wonder what conditions allowed M. psocoides lineage to undergo this specific evolutionary trajectory. Fjellberg (1989) suggested that M. psocoides was adapted to reach food in the inter-leaf spaces of the mosses. In general, it is clear that M. psocoides gained a much slender profile compared to Sphaeridia, from body elongation and size reduction. The straightening of the head and the reduction of anterior trichobothria may indeed allow M. psocoides to reach as far as possible into reducing spaces. The persistence of one anterior trichobothria in the male complicates this straightforward scenario: perhaps the male focuses more on finding females than feeding (the male is also even smaller than the female).

5. Conclusion

By solving the phylogenetic placement of M. psocoides, we demonstrated that the species evolved from one of the most advanced globular body shapes observed in Symphypleona toward an elongated morphology. While adapting to a specialized lifestyle in drought exposed habitat, a globular Sphaeridia-like ancestor made an evolutionary U-turn to reacquire an elongated body and straighten up its head. Neotenic processes probably took part in M. psocoides evolution. Indicators of its success are the wide distribution of M. psocoides on earth, and its ability to occupy a niche in habitats dominated by ancestrally elongated species, such as the drought resistant species F. angularis. We assign Mackenziella psocoides to family Sminthurididae and classify it in the newly established subfamily Sphaeridiainae, together with Sphaeridia.

6. Data availability

The ten novel DNA sequences are deposited on GenBank (, accession numbers for the whole dataset are provided in Table 1. Retrieved nuclear rDNA sequences, alignment and parameter files for the phylogenetic analysis, datation and ancestral character states estimation (IQTREE2, BEAST and PHYTOOLS) are deposited in Zenodo (

7. Acknowledgments

The authors have no funding to report. The authors have declared that no competing interests exist. We express our warm thanks to Andreas Kauk (SMNG, Soil Zoology Department) for helping with the wet lab work. We also warmly thank Leonie Schardt and Pr. Dr. Miklós Bálint (Functional Environmental Genomics Group, LOEWE-TBG) for supporting us with sequencing. Leonie Schardt did the library preparation and sequencing. We thank Dr. Volker Otte (SMNG) for the identification of the mosses. We acknowledge the Metainvert project (led by Pr. Dr. Miklós Bálint and Dr. Ricarda Lehmitz, Senckenberg and LOEWE TBG) for the anticipated access to the genetic resources of some of the springtails species. We wish to thank Géraldine Toutirais of the MNHN’s Plateau Technique de Microscopie Électronique et de Microanalyses for her invaluable help with the SEM.

We thank our reviewers, Frans Janssens and anonymous, as well as the scientific editor, Martin Fikácek, for the excellent discussions and the thoughtful criticisms that improved the manuscript. Frans Janssens attracted our attention on the evolution of the eye of Mackenziella by suggesting one of the alternative hypotheses, and made us aware of the homonymy between Sphaeridiinae Richard, 1968 (Collembola: Sminthurididae) with Sphaeridiinae Latreille, 1802 (Coleoptera: Hydrophilidae).

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Supplementary materials

Supplementary material 1 

Tables S1

Schneider C, D'Haese CA (2023)

Data type: .csv

Explanation note: Matrix of morphological character for the species of Symphypleona represented in this study, used to describe the evolution of Mackenziella psocoides and its last common ancestor with Sphaeridia pumilis.

This dataset is made available under the Open Database License ( The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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Supplementary material 2 

Table S2

Schneider C, D'Haese CA (2023)

Data type: .csv

Explanation note: Species body size data used for the ancestral character estimation.

This dataset is made available under the Open Database License ( The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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Supplementary material 3 

Table S3

Schneider C, D'Haese CA (2023)

Data type: .csv

Explanation note: Known records of Mackenziella psocoides, compiled from litterature and from Edaphobase.

This dataset is made available under the Open Database License ( The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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Supplementary material 4 

Figure S1

Schneider C, D'Haese CA (2023)

Data type: .pdf

Explanation note: Maximum Likelihood tree computed with IQTREE2. Node labels as: nonparametric boostrap/aLRT.

This dataset is made available under the Open Database License ( The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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Supplementary material 5 

Figure S2

Schneider C, D'Haese CA (2023)

Data type: .pdf

Explanation note: Maximum clade credibility tree and age estimates computed with BEAST2, age estimates in right position to the nodes, values in bracket and blue bars indicate 95% HPD intervals of the age estimates.

This dataset is made available under the Open Database License ( The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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Supplementary material 6 

Figure S3

Schneider C, D'Haese CA (2023)

Data type: .pdf

Explanation note: Ancestral body size estimated with the ACE function of Phytools. Full output available in the Zenodo repository (

This dataset is made available under the Open Database License ( The Open Database License (ODbL) is a license agreement intended to allow users to freely share, modify, and use this Dataset while maintaining this same freedom for others, provided that the original source and author(s) are credited.
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