Variations are a-i=Outgroups included, Paraulacini are coded as parasitoids, uncertain taxa coded as parasitoids; a-ii=Outgroups included, Paraulacini are coded as inquilines, uncertain taxa coded as parasitoids; b-i=Outgroups excluded, Paraulacini are coded as parasitoids, uncertain taxa coded as parasitoids; b-ii=Outgroups excluded, Paraulacini are coded as inquilines, uncertain taxa coded as parasitoids; c-i=Outgroups included, Paraulacini are coded as parasitoids, uncertain taxa coded as unknown; c-ii=Outgroups included, Paraulacini are coded as inquilines, uncertain taxa coded as unknowns; d-i=Outgroups excluded, Paraulacini are coded as parasitoids, uncertain taxa coded as unknowns; d-ii=Outgroups excluded, Paraulacini are coded as inquilines, uncertain taxa coded as unknowns. PubMedGoogle Scholar. clade. Genome Biol. [7] and Peters et al. MLB and BBB led the manuscript writing. The evolution of parasite genomes and the origins of parasitism 1989; 33. We selected a 50%, 60% and 70% taxon complete set of loci (containing loci with alignment data from at least 63, 75 and 88 of 126 taxa, and retaining 1147, 918 and 626 UCE loci for analysis, respectively) for further analyses using the script phyluce_align_get_only_loci_with_min_taxa. In: Ecology, and evolution of gall-inducing arthropods. The relationships between members of this clade otherwise remain stable. The same issue was encountered here with UCE data. In the majority of populations, mutualism was . Additional trees estimated from partitioned concatenated analyses. Bootstrap support values are displayed next to respective nodes. Evolution of mutualism from parasitism in experimental virus Analyses were rooted with Ibalia anceps and excluded non-cynipoid outgroups. parasitism, relationship between two species of plants or animals in which one benefits at the expense of the other, sometimes without killing the host organism. We used phyluce_assembly_get_match_counts.py to generate a list of UCE loci shared across all taxa, which was then used to create separate FASTA files for each UCE locus containing sequence data for taxa present at that particular locus, using phyluce_assembly_get_fastas_from_match_counts.py. 2006;103:181727. Phylogenetic relationships and time-calibration of the South American fossil and extant species of southern beeches (Nothofagus). Wiley-Blackwell; 2017. p. 419461. Introduction to the Ecology, Epidemiology, and Evolution of Parasitism Two monotypic cynipoid taxa were not available for this study, Austrocynipidae and Qwaqwaiini, due to their rarity. 3b), with the best alternative being a herb-galling ancestor. Likewise, since larger Hymenoptera studies by Heraty et al. Considering these close affinities, obviously one cannot readily interpret the cynipid evolutionary tree without a comprehensive figitid phylogeny. [18] that a critical bridge between the earlier branching gall-associated figitids and the more derived figitids is a period associated with the aphid community. Madagascar: Ministre de l'Environnement et des Forts, Madagascar National Parks. Mol Biol Evol. It is possible that other intrinsic characteristics of the UCE loci in our data set are responsible for the observed patterns, which are imperfectly (or not at all) correlated with GC content. Phylogeny of Cynipoidea. Following this introduction, Chapter 2 gives a general summary of Daphnia biology, highlighting at the same time those aspects that may be relevant for the study of parasitism. Secondly, we investigated whether the position of E. niger could be the result of particular characteristics of this data set and its locus and taxon composition. Cambier S, Ginis O, Moreau SJ, Gayral P, Hearn J, Stone G, David G, Huguet E, Drezen J-M. Gall wasp transcriptomes unravel potential effectors involved in molecular dialogues with oak and rose bushes. They find that recent waves of migration disseminated the parasite from Old to New World and identify a unique haplotype that likely accompanied the global expansion of cats and is today common to all intercontinental lineages and hybrid populations. [20], but our data present much-needed improved resolution along the backbone of the tree. 8995Ma (Fig. A new subfamily of Figitidae (Hymenoptera, Cynipoidea). As noted above, the GC content across all taxa in our data set did not vary greatly (0.400.46 among ingroup taxa), and GC content for E. niger was on the lower end of this spectrum (0.41, Additional file 2). CAS The placement of the superfamily within the larger Proctotrupomorpha (a clade also containing superfamilies Platygastroidea, Proctotrupoidea, Chalcidoidea and Diapriioidea) has generally been accepted, albeit no previous analyses of cynipoid relationships have included members of other Proctotrupomorpha as outgroups. Overall, the three-state model does not support the hypothesis that parasitoidism was retained from a common ancestor with Platygastroidea, but suggests one or two origins of parasitoidism later in the evolution of Cynipoidea. Sauquet H, Ho SY, Gandolfo MA, Jordan GJ, Wilf P, Cantrill DJ, Bayly MJ, Bromham L, Brown GK, Carpenter RJ. Buffington ML, Nylander JA, Heraty JM. Data processing relied on scripts within the PHYLUCE package v1.5 (Faircloth 2016). of individual parasites that infect the host, i.e. The relationship of Charipinae to core Figitidae has been supported by all previous analyses since Buffington et al. We had filtered our alignments according to three different levels of taxon completeness (50%, 60% and 70%), meaning a locus had to be recovered in a certain percentage of the taxa to be retained. 2019;19:153144. Nearly all cynipine genera sampled here were found to be not monophyletic in our analyses, and clearly a Cynipini-focused analysis will be needed to work out generic boundaries within the tribe. Syst Entomol. b 7-state set, with states 0/grey=parasitoid, 1/orange=inquiline and 2/dark-blue=galler-Fagaceae, 3/green=galler-herbs, 4/light-brown=galler-Acer, 5/light-blue=galler-Rosaceae, 6/red=galler-Acacia. BMC Evol Biol 20, 155 (2020). We pruned all but two closest outgroups (Platygaster sp. Cruaud A, Nidelet S, Arnal P, Weber A, Fusu L, Gumovsky A, Huber J, Polaszek A, Rasplus JY. Please be respectful of copyright. Cookies policy. Males attach themselves to females with their jaws, and in some cases the tissues and circulatory systems between the sexes are joined. In the ML-unpart-50 tree, Phanacis is placed as sister to the clade consisting of Cynipini, Ceroptresini, Diastrophini, and Synergini, but this grouping is basically unsupported (BS=45). Ancestral state reconstructions of cynipoid life histories using a seven-state model. Mol Phylogenet Evol. For clade I (Paraulacini), estimations are unchanged compared to the three-state model, with estimates either suggesting a parasitoid or an inquiline MRCA with highest probability (node 110, Fig. PLoS ONE. B: Sketch of the main topology recovered by Ronquist et al. and Platygaster sp. The concentrations of our DNA extractions ranged from<0.05ng/L to 27.4ng/L (average 2.9ng/L), due to variable specimen size and age range. 2 and Table 1: node 161) within the same geological time period. Transcriptome sequence-based phylogeny of chalcidoid wasps (Hymenoptera: Chalcidoidea) reveals a history of rapid radiations, convergence, and evolutionary success. 2018;35:1798811. [20] and also supported by our data, either the basal position of Eschatocerini as sister-group to all cynipoids, or Eschatocerini being sister-group to figitids are plausible. Or get a Premium Subscription to access the best of Nat Geo - just $19, Controversial oil drilling paused in Namibian wilderness, Dolphin moms use 'baby talk' with their calves, Nevada is crawling with swarms of smelly 'Mormon crickets'. Here, the authors produce whole genome sequences of modern and ancient samples from humans and non-human primates to characterise the genomic diversity and evolution of this pathogen. Princeton: Princeton University Press; 1994. Taxon labels are colored by their terminals state; select node are labeled with numbers corresponding to Additional file 14 and 15. Median crown age estimates for Cynipoidea center around 190Ma (Fig. Episodic radiations in the fly tree of life. Wiegmann et al. There are three firsts in our dataset that may have contributed to the novel relationships recovered: proper outgroup sampling, a genome-scale data set, and comprehensive ingroup sampling. The morphology of these wasps is extremely apomorphic: species lack mandibles; their cuticle is very thin and pale yellow; the wings have a mere suggestion of the marginal cell; and lastly, they gall Acacia and Prosopis (Fabaceae) in semi-arid regions of South America. Analyses were rooted using the outgroup method and our outer outgroup taxon Callihormius bifasciatus (Braconidae). Adams RH, Castoe TA. Parasites provide a framework for understanding specialization. [43] estimated stem-group siricoids, the presumed hosts of proto-ibaliids, to be Triassic in age, suggesting our estimates here are perhaps too young and influenced by restricted taxon sampling. Hipp AL, Manos PS, Gonzlez-Rodrguez A, Hahn M, Kaproth M, McVay JD, Avalos SV, Cavender-Bares J. Sympatric parallel diversification of major oak clades in the Americas and the origins of Mexican species diversity. A deeper meaning for shallowlevel phylogenomic studies: nested anchored hybrid enrichment offers great promise for resolving the tiger moth tree of life (Lepidoptera: Erebidae: Arctiinae). Heraty JM, Burks RA, Cruaud A, Gibson GA, Liljeblad J, Munro J, Rasplus JY, Delvare G, Janta P, Gumovsky A. 2007;24:158691. Support values are local posterior probabilities, which are branch support values that measure the support for a quadripartition, not a bipartition. We used the with-bead approach for PCR recovery of enriched libraries as described in Faircloth et al. A cabbage butterfly caterpillar stands watch over white butterfly wasp cocoons, a common parasite that kills its caterpillar hosts by eating them from the inside out. We see strong support for the agastoparasitism hypothesis [where host and parasite are close relatives of each other, suggesting there are shared physiological traits among the two species; 13] regarding Synophromorpha, Periclistus and Diastrophus, where Diastrophus are gall-inducers, and the other two genera inquilines of these inducers. [43]. Our study has significant impact on understanding cynipoid evolution and highlights the importance of adequate outgroup sampling. PubMed Central Specimens collected within the past twenty years were chosen first, but older specimens (oldest dating to 1935) were also included when younger specimens were not available. Perhaps the very nature of the biology of Ibalia, with its switch to being a wood-boring insect parasitoid, has shaped its morphology and thus resulted in an archaic-looking wasp, morphologically more akin to other wood-boring hymenopterans. The rapid diversification within Cynipini is also evidenced by the very short internal branches estimated in the maximum likelihood analyses (Fig. Evaluating alternative hypotheses for the early evolution and diversification of ants. 2015;15:489501. 1999;28:1350. Given these previous results, they could either fall into an early branching grade of gall wasps, or be included within the core cynipids, among the herb gallers and woody rosid gallers. Cambier et al. 2 and Table 1: node 221). Similar to clade ii, crown Figitidae s.l. Ultraconserved elements show utility in phylogenetic inference of Adephaga (Coleoptera) and suggest paraphyly of Hydradephaga. Syst Entomol. Second, the influence of outgroup choice on tree topology and ingroup relationships is well documented in phylogenetics [e.g., 25, 26, 27]. Revision and phylogenetics of the genus Paraulax Kieffer (Hymenoptera, Cynipidae) with biological notes and description of a new tribe, a new genus, and five new species. Most nodes have bootstrap support=100; ranges represent variation in support across analyses. Parallel comparisons of other parasites suggest we need to rethink the drivers and consequences of the parasitic lifestyle. Calibration points used in this study and their justification. For example, we consistently found Euceroptrinae as sister-group to Liopteridae, but never Euceroptrinae grouping with the other gall-associated figitids [as in 18]. Bioinformatics. As our main phylogenetic result, we therefore summarize major subfamily and tribal relationships recovered by the partitioned analysis of the 50% completeness matrix (ML-part-50; shown in Fig. From Michelin-starred menus to gilded historic sites, these restaurants are worth a visitwhether or not youre a tourist. As these internal branches are relatively short (Fig. 2019;44:51426. Using comprehensive ingroup and outgroup sampling, our study has clarified certain hypotheses in cynipoid evolution, as outlined above. 3a and Additional file 14). Phylogeny and classification of Hymenoptera. Massachusetts: Harvard University Press; 1990. Bossert S, Murray EA, Blaimer BB, Danforth BN. Mol Biol Evol. By reconstructing a robust phylogeny and highlighting patterns of life histories, our study has established the framework for further physiological and comparative genomic work between gall-making, inquiline and parasitoid lineages in this fascinating system, and will have many implications for the evolution of parasitism and other life histories in Hymenoptera. Liu Z, Engel MS, Grimaldi DA. Buffington ML, Liljeblad J. I point out which features of parasites make them attractive ecological factors and why the study of parasites may add to our understanding of Daphnia biology. Four tribes render Cynipidae paraphyletic: Eschatocerini, Paraulacini, Pediaspidini and Diplolepidini. Here's what you should know. Article These Gettysburg maps reveal how Lee lost the fight, Who is Oppenheimer? [28], Sharkey et al. We also find here a much younger age for the split of Paramblynotus (Oriental) and Oberthuerella+Pseudibalia (ca. Updates? Acta Palaeontol Pol. Our data continue to support a perspective previously discussed by Ronquist [15] and Buffington et al. Considering these shared molecular characteristics in light of our phylogeny and ancestral reconstructions (Figs. The SH test did not detect a significantly better likelihood score for the tree estimated by rooting with Paraulax versus rooting with Ibalia versus specifying no outgroup at all. Syst Biol. The whipworm Trichuris trichiura is a soil-transmitted helminth that causes the neglected tropical disease trichuriasis in humans. The authors declare that they have no competing interests. 2000;17:54052. Position B is most prevalent in bins with high (0.510.64) and medium GC content (0.440.47), whereas position A is recovered from a variety of GC contents. Phylogeny, evolution and classification of gall wasps: the plot thickens. We also included seven taxa from other Hymenoptera lineages with varying degree of relatedness to cynipoid wasps: four platygastroid taxa (Sparasion cullaris, Nixonia watshami, Trissolcus sp. Because of their short generation times and large population sizes, parasites can evolve rapidly. CAS 2015;16:124. Besides the characteristic forms of insect-specific carnivory or entomophagy, some parasitoid Hymenoptera (Cynipoidea, Chalcidoidea, a few Braconidae, and a few sawflies) have diversified to use plant tissues as their hosts. This two-volume edited book highlights and reviews the potential of the fossil record to calibrate the origin and evolution of parasitism, and the techniques to understand the development of parasite-host associations and their relationships with environmental and ecological changes. These bug repellents actually workif you use them correctly, People with ADHD struggle to stay afloat amid drug shortage, A supersonic jet chased a solar eclipse across Africafor science. 2019;10:926. BRIEF COMMUNICATION doi:10.1111/evo.13440 Evolution of mutualism from parasitism in experimental virus populations Jason W. Shapiro 1,2,3 and Paul E. Turner 1,4 1 Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut 06520 2 Current Address: Department of Biology, Loyola University Chicago, 1032 W Sheridan Rd., Chicago, Illinois 60660 Bioscience. Google Scholar. Summary The first comparison of parasitic trypanosomatids to their free-living relatives reveals that some characteristics once linked to parasitism actually predate it. 2012;28:80112. Cladistics. re-write the evolution of parasitism within cynipoid wasps Bonnie B. Blaimer1,2,3*, Dietrich Gotzek2, Sen G. Brady2 and Matthew L. Bungton 4* Abstract Background: Parasitoidism, a specialized life strategy in which a parasite eventually kills its host, is frequently found within the insect order Hymenoptera (wasps, ants and bees). Sauquet et al. Phylogenetic Insights into the Evolution of Parasitism in Hymenoptera 2016;16:1189203. If we remove the platygastroid and other outgroups from the analysis and root with Ibalia (Additional file 9A), we return to a topology that nearly resembles those of previous family-level analyses [Additional file 9B,C; see 17, 18, 20]. Zool Scr. In a larger Hymenoptera UCE-based analysis (Blaimer et al. Phylogenomic analyses utilized the Smithsonian Institution High Performance Cluster (SI/HPC). These novel relationships were robust and well-supported in all our analyses and with respect to different analytical parameters. Main tree is displayed as cladogram for clarity of relationships (left panel); right panel shows phylogram including information on branch lengths. Animals Have Evolved Into Parasites At Least 200 Times We surmise that the novel positions of Paraulacini and Diplolepidini/Pediaspidini as earliest branching taxa, and Ibaliidae and Liopteridae as derived members of Cynipoidea, are indeed the result of proper outgroup taxon sampling and correct rooting in our analyses. 2012;22:93946. are lethal inquilines sensu Nieves-Aldrey [40]). Subsequent higher-level diversification within this clade happened fairly fast within the next 1025 million years within the early Cretaceous. The controversial man behind the atomic bomb. 1). Lanfear R, Frandsen PB, Wright AM, Senfeld T, Calcott B. PartitionFinder 2: New methods for selecting partitioned models of evolution for molecular and morphological phylogenetic analyses. PubMed Central Libraries had post-PCR concentrations from 0.131.6ng/L. Comparative genomics of all known Laverania species that infect African great apes reveals interspecies gene transfer and convergent evolution, and identifies features of Plasmodium falciparum, the only human-infective species within this subgenus, that may have led to its speciation and spread globally. Between<5ng and 567ng DNA was sheared for 060 secs (amp=25, pulse=10) to a target size of approximately 500600bp by sonication (Q800, Qsonica Inc., Newtown, CT) and used as the input for a modified genomic DNA library preparation protocol (Kapa Hyper Prep Library Kit, Kapa Biosystems, Wilmington, MA) that incorporated with-bead cleanup steps [66] and a generic SPRI substitute [67]. Gahan AB. Evolution of mutualism from parasitism in experimental virus - JSTOR 2 and Table 1: node 220) to have originated in the early Cretaceous; in contrast, crown-group Diplolepidini (the rose gallers) have an Eocene origin and are only about 39Ma old (Fig. Nylander JA, Ronquist F, Huelsenbeck JP, Nieves-Aldrey J. Bayesian phylogenetic analysis of combined data. Summarized here are identical topologies resulting from unpartitioned Maximum Likelihood analyses with IQ-TREE (combined ML search for best tree and 1000 bootstraps) of 50%, 60% and 70% completeness matrices including 119 ingroup taxa. ), one species of Eulophidae (Leptocybe invasa), one species of Diapriidae (Propsilomma columbianum) and one braconid species (Callihormius bifasciatus). A parasitoid lifestyle is one of two dominant life strategies within the hymenopteran superfamily Cynipoidea, with the other being an unusual plant-feeding behavior known as galling. than enhance understanding of the evolution of parasitism. Branstetter MG, Danforth BN, Pitts JP, Faircloth BC, Ward PS, Buffington ML, Gates MW, Kula RR, Brady SG. Bootstrap support values are displayed next to respective nodes. Research on figitids began in earnest with Fontal-Cazalla et al. Summary of phylogenetic positions for Eschatocerus niger. We investigated this variation by binning our UCE loci depending on their GC content, and performed phylogenetic inference (ML-IQTREE analyses) on a concatenated matrix from each bin. Hill RS. Genomic dissection of an extended phenotype: Oak galling by a cynipid gall wasp. The funding bodies had no role in the design of the study and collection, analysis, and interpretation of data and in writing the manuscript. A phylogenetic analysis of the megadiverse Chalcidoidea (Hymenoptera). 2011;12:R1. Peters RS, Niehuis O, Gunkel S, Blser M, Mayer C, Podsiadlowski L, Kozlov A, Donath A, van Noort S, Liu S, et al. Target enrichment of ultraconserved elements from arthropods provides a genomic perspective on relationships among Hymenoptera. First published: 23 March 2022 https://doi.org/10.1111/evo.14457 Citations: 1 Sections PDF Tools Share Abstract Colonies of social insects contain large amounts of resources often exploited by specialized social parasites. 2011;29:64452. Position C is only recovered by two bins with low GC content (0.370.41), but results from the lowest GC content recover E. niger again in position A (0.260.37). Analyses were rooted using the outer outgroup Callihormius bifasciatus. All trees are presented as cladograms for clarity of relationships, and are based on a combined ML search for the best tree and 1000 bootstrap replicates using unpartitioned data matrices. We chose not to perform statistical binning [82] prior to gene tree estimation due to concerns about this procedure [83]. 2004;53:4767. Evolution of Parasitism - UC Davis Parasitoidism, a specialized life strategy in which a parasite eventually kills its host, is frequently found within the insect order Hymenoptera (wasps, ants and bees). Lastly, we found support for the agastoparasitism hypothesis [13], with the inquilinous genera Synophromorpha and Periclistus being close relatives of their host genus Diastrophus. From the enriched libraries, we were able to generate 219,39121,713,730 raw sequencing reads per taxon (average: 3,134,133), which were assembled into 2,697275,787 contigs (average: 51,162) with Trinity, of average length 254394bp per taxon (average: 314bp).

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