The Chalcidoidea bush of life: evolutionary history of a massive radiation of minute wasps.

Chalcidoidea are mostly parasitoid wasps that include as many as 500 000 estimated species. Capturing phylogenetic signal from such a massive radiation can be daunting. Chalcidoidea is an excellent example of a hyperdiverse group that has remained recalcitrant to phylogenetic resolution. We combined 1007 exons obtained with Anchored Hybrid Enrichment with 1048 ultra-conserved elements (UCEs) for 433 taxa including all extant families, >95% of all subfamilies, and 356 genera chosen to represent the vast diversity of the superfamily. Going back and forth between the molecular results and our collective knowledge of morphology and biology, we detected bias in the analyses that was driven by the saturation of nucleotide data. Our final results are based on a concatenated analysis of the least saturated exons and UCE datasets (2054 loci, 284 106 sites). Our analyses support an expected sister relationship with Mymarommatoidea. Seven previously recognized families were not monophyletic, so support for a new classification is discussed. Natural history in some cases would appear to be more informative than morphology, as illustrated by the elucidation of a clade of plant gall associates and a clade of taxa with planidial first-instar larvae. The phylogeny suggests a transition from smaller soft-bodied wasps to larger and more heavily sclerotized wasps, with egg parasitism as potentially ancestral for the entire superfamily. Deep divergences in Chalcidoidea coincide with an increase in insect families in the fossil record, and an early shift to phytophagy corresponds with the beginning of the "Angiosperm Terrestrial Revolution". Our dating analyses suggest a middle Jurassic origin of 174 Ma (167.3-180.5 Ma) and a crown age of 162.2 Ma (153.9-169.8 Ma) for Chalcidoidea. During the Cretaceous, Chalcidoidea may have undergone a rapid radiation in southern Gondwana with subsequent dispersals to the Northern Hemisphere. This scenario is discussed with regard to knowledge about the host taxa of chalcid wasps, their fossil record and Earth's palaeogeographic history

A revision of the <i>Encarsia mexicana</i> species-group (=<i>Dirphys</i> Howard) (Hymenoptera: Aphelinidae), gregarious endoparasitoids of whiteflies (Hemiptera: Aleyrodidae) in the Neotropical Region

The genus Dirphys Howard 1914 syn. n. is synonymized with Encarsia Förster, and treated as a species-group of Encarsia, referred to henceforth as the Encarsia mexicana species-group. The monophyly of Encarsia is discussed in relation to Dirphys. The new synonymy is based on phylogenetic analyses of the nuclear ribosomal 28S-D2 gene region (43 taxa, 510 bp). The Encarsia mexicana species-group is recovered as strongly monophyletic within Encarsia. All species of the Encarsia mexicana species-group are revised. The group includes six previously described species, and fourteen newly described species. All species are described (or redescribed) and illustrated. Detailed distributional data, and, where available, plant associate and host records are provided for all species. Encarsia myartsevae Kresslein and Polaszek nom. nov. is here proposed as a replacement name for Encarsia mexicana Myartseva, now preoccupied by Encarsia mexicana (Howard). A dichotomous identification key, supplemented by an online multiple-entry key, is provided for all species

Fig. 5 in The Chalcidoidea bush of life: evolutionary history of a massive radiation of minute wasps

Fig. 5. Global historical biogeography of Chalcidoidea and new classification. The chronogram obtained from the complete set of ingroup taxa is illustrated. The previous classification is used to annotate tips (four letter prefixes; see also Table S1 for complete information on sampling) with successive grey and white boxes grouping the tip labels. The new familial classification from Burks et al. (2022) is shown to the right. For clarity, ancestral ranges are given only up to family level and only for the BAYEAREALIKE + J model (which was selected by AICc). All inferences of ancestral ranges are provided in Fig. S5. Inferences of ancestral ranges were conducted with only one specimen per genus as shown with brackets that connect tips. Current distribution of genera is shown with coloured boxes at tips. Sampling area of specimens is indicated in tip labels. NEO = Neotropical; NEA = Nearctic; AFR = Afrotropical; PAL = Palaearctic; ORI = Oriental; AUS = Australasian. UKN = Unknown when collection data are unavailable. Stars indicate that specimens were sampled in areas where species was introduced or not yet cited. Sampling area for the specimen used for sequencing exons is listed first, sampling area for the specimen used for sequencing UCEs is listed second; n.a. is used when no specimen was sequenced and only one sampling area is reported when exons and UCEs were obtained from specimens sampled in the same areas (or from the same specimen). Unless specified, nodes are supported by SHaLRT ≥80%, UFBoot ≥95% and sCF ≥34.3 (minimum support for a family that is well defined morphologically, Trichogrammatidae). Nodes with a grey circle are supported by SHaLRT &lt;80% or UFBoot &lt;95%; nodes with a black circle are supported by SHaLRT &lt;80% and UFBoot &lt;95%; nodes with a black triangle are supported with sCF &lt;34.3. Images on the left of tentative family names are all at the same scale. Images on the right of tentative family names have been magnified. Photos ©K. Bolte (Baeomorphidae); ©J.-Y. Rasplus (all others).Published as part of &lt;i&gt;Cruaud, Astrid, Rasplus, Jean-Yves, Zha, Junxia, Burks, Roger, Delvare, Ǵerard, Fusu, Lucian, Gumovsky, Alex, Huber, John T., Jan̆sta, Petr, Mitroiu, Mircea-Dan, Noyes, John S., Noort, Simon van, Baker, Austin, Bohmova, Julie, Baur, Hannes, Blaimer, Bonnie B., Brady, Sean G., Bubeńıkova, Kristyna, Chartois, Marguerite, Copeland, Robert S., Papilloud, Natalie Dale-Skey, Molin, Ana Dal, Dominguez, Chrysalyn, Gebiola, Marco, Guerrieri, Emilio, Kresslein, Robert L., Krogmann, Lars, Lemmon, Emily, Murray, Elizabeth A., Nidelet, Sabine &amp; Nieves-Aldrey, Jośe Luis, 2023, The Chalcidoidea bush of life: evolutionary history of a massive radiation of minute wasps, pp. 1-30 in Cladistics 2023&lt;/i&gt; on page 15, DOI: 10.1111/cla.12561, &lt;a href="http://zenodo.org/record/10115140"&gt;http://zenodo.org/record/10115140&lt;/a&gt

The Chalcidoidea bush of life: evolutionary history of a massive radiation of minute wasps

Cruaud, Astrid, Rasplus, Jean-Yves, Zha, Junxia, Burks, Roger, Delvare, Ǵerard, Fusu, Lucian, Gumovsky, Alex, Huber, John T., Jan̆sta, Petr, Mitroiu, Mircea-Dan, Noyes, John S., Noort, Simon van, Baker, Austin, Bohmova, Julie, Baur, Hannes, Blaimer, Bonnie B., Brady, Sean G., Bubeńıkova, Kristyna, Chartois, Marguerite, Copeland, Robert S., Papilloud, Natalie Dale-Skey, Molin, Ana Dal, Dominguez, Chrysalyn, Gebiola, Marco, Guerrieri, Emilio, Kresslein, Robert L., Krogmann, Lars, Lemmon, Emily, Murray, Elizabeth A., Nidelet, Sabine, Nieves-Aldrey, Jośe Luis (2023): The Chalcidoidea bush of life: evolutionary history of a massive radiation of minute wasps. Cladistics 2023: 1-30, DOI: 10.1111/cla.1256

Fig. 1 in The Chalcidoidea bush of life: evolutionary history of a massive radiation of minute wasps

Fig. 1. Comparison of properties of the analysed datasets. Datasets (AHE414 and UCEs) are described in Table 1. For each panel, letters above box plots reflect pairwise comparisons of marginal means estimated from the best-fit models; distributions sharing a letter do not differ significantly. Points: raw data (Table S2a). In (e), saturation was assessed by calculating the R2 of the linear regression of uncorrected p-distances against inferred distances in individual gene trees. Highest R2 are for least saturated loci. The scale of the Y axis is reversed to better show decrease in saturation. (f) The convergence of trees as saturation decreases. The Y axis shows the relative RF distance between pairs of trees obtained with either the combined exons or the combined UCEs. The X axis show the absolute value of the difference between the medians of the R2 of the linear regression of uncorrected p-distances against inferred distances in gene trees that were combined to get the compared trees [cf. (e)]. Four comparisons were performed in each case as datasets were analysed with and without partitioning.Published as part of &lt;i&gt;Cruaud, Astrid, Rasplus, Jean-Yves, Zha, Junxia, Burks, Roger, Delvare, Ǵerard, Fusu, Lucian, Gumovsky, Alex, Huber, John T., Jan̆sta, Petr, Mitroiu, Mircea-Dan, Noyes, John S., Noort, Simon van, Baker, Austin, Bohmova, Julie, Baur, Hannes, Blaimer, Bonnie B., Brady, Sean G., Bubeńıkova, Kristyna, Chartois, Marguerite, Copeland, Robert S., Papilloud, Natalie Dale-Skey, Molin, Ana Dal, Dominguez, Chrysalyn, Gebiola, Marco, Guerrieri, Emilio, Kresslein, Robert L., Krogmann, Lars, Lemmon, Emily, Murray, Elizabeth A., Nidelet, Sabine &amp; Nieves-Aldrey, Jośe Luis, 2023, The Chalcidoidea bush of life: evolutionary history of a massive radiation of minute wasps, pp. 1-30 in Cladistics 2023&lt;/i&gt; on page 6, DOI: 10.1111/cla.12561, &lt;a href="http://zenodo.org/record/10115140"&gt;http://zenodo.org/record/10115140&lt;/a&gt

Fig. 4 in The Chalcidoidea bush of life: evolutionary history of a massive radiation of minute wasps

Fig. 4. The Chalcidoidea bush of life. (a) IQ-TREE tree obtained from the combined exonsAA+UCEs90-25 datasets (see also Fig. S1). Monophyletic families are in grey, para- or polyphyletic families are in colour. Higher level groups/clades discussed in text are highlighted with boxes. Statistical support for backbone nodes are shown with single (SH-aLRT ≧80% or UFboot ≧95%) or double stars (SH-aLRT ≧80% and UFboot ≧95%). (b) Contribution of the exonsAA and UCEs90-25 datasets to the combined tree. Gene concordance factor (gCF); gene discordance factor due to polyphyly (gDFP); site concordance factor averaged over 100 quartets (sCF). Points: raw data (Table S2d). (c) Comparison of branch length for the backbone nodes and other ingroup nodes. Points: raw data (Table S2c). For (b) and (c), stars above box plots indicate statistical significance: ns, p&gt; 0.05; ***, p ≤ 0.001; ****, p ≤ 0.0001. (d) Correlation between node age and sCF (outgroups excluded). Points: raw data (Table S2e); line: regression curve for the best-fit model (log linear model; p &lt;2.2e—16).Published as part of &lt;i&gt;Cruaud, Astrid, Rasplus, Jean-Yves, Zha, Junxia, Burks, Roger, Delvare, Ǵerard, Fusu, Lucian, Gumovsky, Alex, Huber, John T., Jan̆sta, Petr, Mitroiu, Mircea-Dan, Noyes, John S., Noort, Simon van, Baker, Austin, Bohmova, Julie, Baur, Hannes, Blaimer, Bonnie B., Brady, Sean G., Bubeńıkova, Kristyna, Chartois, Marguerite, Copeland, Robert S., Papilloud, Natalie Dale-Skey, Molin, Ana Dal, Dominguez, Chrysalyn, Gebiola, Marco, Guerrieri, Emilio, Kresslein, Robert L., Krogmann, Lars, Lemmon, Emily, Murray, Elizabeth A., Nidelet, Sabine &amp; Nieves-Aldrey, Jośe Luis, 2023, The Chalcidoidea bush of life: evolutionary history of a massive radiation of minute wasps, pp. 1-30 in Cladistics 2023&lt;/i&gt; on page 13, DOI: 10.1111/cla.12561, &lt;a href="http://zenodo.org/record/10115140"&gt;http://zenodo.org/record/10115140&lt;/a&gt

Fig. 2 in The Chalcidoidea bush of life: evolutionary history of a massive radiation of minute wasps

Fig. 2. Overview of the topologies obtained with the different datasets as saturation decreases. Datasets (AHE414 and UCEs) are described in Table 1, and trees are available in Fig. S1 and Appendix S1. Groups that are discussed in text are highlighted. Only IQ-TREE trees are shown. ROTO/BAEO = Rotoitidae (Baeomorphidae); CHAL = Chalcididae; EURY = Eurytomidae; GALL = gall clade (see text); MYMA = Mymaridae; PTERO = group of Pteromalid wasps (Austroterobiinae; part Colotrechninae; Miscogastrinae; part Ormocerinae; Otitesellinae; Pteromalinae; Sycoecinae; Sycoryctinae); "Tiny Wasp clade" (see text).Published as part of &lt;i&gt;Cruaud, Astrid, Rasplus, Jean-Yves, Zha, Junxia, Burks, Roger, Delvare, Ǵerard, Fusu, Lucian, Gumovsky, Alex, Huber, John T., Jan̆sta, Petr, Mitroiu, Mircea-Dan, Noyes, John S., Noort, Simon van, Baker, Austin, Bohmova, Julie, Baur, Hannes, Blaimer, Bonnie B., Brady, Sean G., Bubeńıkova, Kristyna, Chartois, Marguerite, Copeland, Robert S., Papilloud, Natalie Dale-Skey, Molin, Ana Dal, Dominguez, Chrysalyn, Gebiola, Marco, Guerrieri, Emilio, Kresslein, Robert L., Krogmann, Lars, Lemmon, Emily, Murray, Elizabeth A., Nidelet, Sabine &amp; Nieves-Aldrey, Jośe Luis, 2023, The Chalcidoidea bush of life: evolutionary history of a massive radiation of minute wasps, pp. 1-30 in Cladistics 2023&lt;/i&gt; on page 8, DOI: 10.1111/cla.12561, &lt;a href="http://zenodo.org/record/10115140"&gt;http://zenodo.org/record/10115140&lt;/a&gt

Fig. 3 in The Chalcidoidea bush of life: evolutionary history of a massive radiation of minute wasps

Fig. 3. Collapsed summary cladograms. Combined AHE (exonsAA) and UCE (UCEs90-25) results for 433 taxa, 2054 loci including 103 395 AA +180 711 nucleotide sites. Results of IQ-TREE concatenated analysis with one partition for each type of data (exonsAA vs. UCEs90-25). SHaLRT/UFBoot/gCF/sCF are indicated at nodes. Clades were collapsed to higher level groups (family, subfamily, tribe). Colours are meant to allow for comparisons between trees. Vertical bars represent similar clade relationships for the analyses of IQ-TREE: UCEs90-25 (UCE407), exonsAA (AHE414), AHE520AA; parsimony: combined (COM433), UCEs90-25 (UCE407), exonsAA (AHE414), AHE520AA; Munro et al. (2011; 720 taxa); Heraty et al. (2013; 300 taxa). Vertical red bars with an X were not recovered as monophyletic in that analysis. Faded colour bars represent that the clade was included but relationships alternated. P indicates paraphyletic lineages. Clades without an X or bar were supported; the lack of a bar indicates the clade was supported but the deeper relationships were not. Higher group names refer to the classification before Burks et al. (2022). Family abbreviations expanded in Table S1.Published as part of &lt;i&gt;Cruaud, Astrid, Rasplus, Jean-Yves, Zha, Junxia, Burks, Roger, Delvare, Ǵerard, Fusu, Lucian, Gumovsky, Alex, Huber, John T., Jan̆sta, Petr, Mitroiu, Mircea-Dan, Noyes, John S., Noort, Simon van, Baker, Austin, Bohmova, Julie, Baur, Hannes, Blaimer, Bonnie B., Brady, Sean G., Bubeńıkova, Kristyna, Chartois, Marguerite, Copeland, Robert S., Papilloud, Natalie Dale-Skey, Molin, Ana Dal, Dominguez, Chrysalyn, Gebiola, Marco, Guerrieri, Emilio, Kresslein, Robert L., Krogmann, Lars, Lemmon, Emily, Murray, Elizabeth A., Nidelet, Sabine &amp; Nieves-Aldrey, Jośe Luis, 2023, The Chalcidoidea bush of life: evolutionary history of a massive radiation of minute wasps, pp. 1-30 in Cladistics 2023&lt;/i&gt; on page 9, DOI: 10.1111/cla.12561, &lt;a href="http://zenodo.org/record/10115140"&gt;http://zenodo.org/record/10115140&lt;/a&gt

The Chalcidoidea bush of life: evolutionary history of a massive radiation of minute wasps

Raw paired reads were uploaded as NCBI Sequence Read Archives (PRJNA884376 for AHE and PRJNA1017994 for UCEs).We dedicate this work to the memory of our dear friend and colleague John LaSalle, specialist of Eulophidae, who was an enthusiastic member of this project.International audienceChalcidoidea are mostly parasitoid wasps that include as many as 500 000 estimated species. Capturing phylogenetic signal from such a massive radiation can be daunting. Chalcidoidea is an excellent example of a hyperdiverse group that has remained recalcitrant to phylogenetic resolution. We combined 1007 exons obtained with Anchored Hybrid Enrichment with 1048 ultra-conserved elements (UCEs) for 433 taxa including all extant families, >95% of all subfamilies, and 356 genera chosen to represent the vast diversity of the superfamily. Going back and forth between the molecular results and our collective knowledge of morphology and biology, we detected bias in the analyses that was driven by the saturation of nucleotide data. Our final results are based on a concatenated analysis of the least saturated exons and UCE datasets (2054 loci, 284 106 sites). Our analyses support an expected sister relationship with Mymarommatoidea. Seven previously recognized families were not monophyletic, so support for a new classification is discussed. Natural history in some cases would appear to be more informative than morphology, as illustrated by the elucidation of a clade of plant gall associates and a clade of taxa with planidial first-instar larvae. The phylogeny suggests a transition from smaller soft-bodied wasps to larger and more heavily sclerotized wasps, with egg parasitism as potentially ancestral for the entire superfamily. Deep divergences in Chalcidoidea coincide with an increase in insect families in the fossil record, and an early shift to phytophagy corresponds with the beginning of the “Angiosperm Terrestrial Revolution”. Our dating analyses suggest a middle Jurassic origin of 174 Ma (167.3–180.5 Ma) and a crown age of 162.2 Ma (153.9–169.8 Ma) for Chalcidoidea. During the Cretaceous, Chalcidoidea may have undergone a rapid radiation in southern Gondwana with subsequent dispersals to the Northern Hemisphere. This scenario is discussed with regard to knowledge about the host taxa of chalcid wasps, their fossil record and Earth's palaeogeographic history