Mitochondrial (mt) function depends critically on optimal interactions between components encoded by mt and nuclear DNAs. mitochondrial DNA (mtDNA) inheritance (SMI) is thought to have evolved in animal species to maintain mito-nuclear complementarity by preventing the spread of selfish mt elements thus typically rendering mtDNA heteroplasmy evolutionarily ephemeral. Here, we show that mtDNA intraorganismal heteroplasmy can have deterministic underpinnings and persist for hundreds of millions of years. We demonstrate that the only exception to SMI in the animal kingdom, that is, the doubly uniparental mtDNA inheritance system in bivalves, with its three-way interactions among egg mt-, sperm mt- and nucleus-encoded gene products, is tightly associated with the maintenance of separate male and female sexes (dioecy) in freshwater mussels. Specifically, this mother-through-daughter and father-through-son mtDNA inheritance system, containing highly differentiated mt genomes, is found in all dioecious freshwater mussel species. Conversely, all hermaphroditic species lack the paternally transmitted mtDNA (=possess SMI) and have heterogeneous macromutations in the recently discovered, novel protein-coding gene (F-orf) in their maternally transmitted mt genomes. Using immunoelectron microscopy, we have localized the F-open reading frame (ORF) protein, likely involved in specifying separate sexes, in mitochondria and in the nucleus. Our results support the hypothesis that proteins coded by the highly divergent maternally and paternally transmitted mt genomes could be directly involved in sex determination in freshwater mussels. Concomitantly, our study demonstrates novel features for animal mt genomes: the existence of additional, lineage-specific, mtDNA-encoded proteins with functional significance and the involvement of mtDNA-encoded proteins in extra-mt functions. Our results open new avenues for the identification, characterization, and functional analyses of ORFs in the intergenic regions, previously defined as "noncoding," found in a large proportion of animal mt genomes.
Hemiptera, the largest non-holometabolous order of insects, represents approximately 7% of metazoan diversity. With extraordinary life histories and highly specialized morphological adaptations, hemipterans have exploited diverse habitats and food sources through approximately 300 Myr of evolution. To elucidate the phylogeny and evolutionary history of Hemiptera, we carried out the most comprehensive mitogenomics analysis on the richest taxon sampling to date covering all the suborders and infraorders, including 34 newly sequenced and 94 published mitogenomes. With optimized branch length and sequence heterogeneity, Bayesian analyses using a site-heterogeneous mixture model resolved the higher-level hemipteran phylogeny as (Sternorrhyncha, (Auchenorrhyncha, (Coleorrhyncha, Heteroptera))). Ancestral character state reconstruction and divergence time estimation suggest that the success of true bugs (Heteroptera) is probably due to angiosperm coevolution, but key adaptive innovations (e.g. prognathous mouthpart, predatory behaviour, and haemelytron) facilitated multiple independent shifts among diverse feeding habits and multiple independent colonizations of aquatic habitats.
Three new genera are described: Michener (Proteropinae), Bioalfa (Rogadinae), and Hermosomastax (Rogadinae). Keys are given for the New World genera of the following braconid subfamilies: Agathidinae, Braconinae, Cheloninae, Homolobinae, Hormiinae, Ichneutinae, Macrocentrinae, Orgilinae, Proteropinae, Rhysipolinae, and Rogadinae. In these subfamilies 416 species are described or redescribed. Most of the species have been reared and all but 13 are new to science. A consensus sequence of the COI barcodes possessed by each species is employed to diagnose the species, and this approach is justified in the introduction. Most descriptions consist of a lateral or dorsal image of the holotype, a diagnostic COI consensus barcode, the Barcode Index Number (BIN) code with a link to the Barcode of Life Database (BOLD), and the holotype specimen information required by the International Code of Zoological Nomenclature. The following species are treated and those lacking authorship are newly described here with authorship attributable to Sharkey except for the new species of Macrocentrinae which are by Sharkey & van Achterberg: AGATHIDINAE: Aerophilus paulmarshi, Mesocoelus davidsmithi, Neothlipsis bobkulai, Plesiocoelus vanachterbergi, Pneumagathis erythrogastra (Cameron, 1905), Therophilus bobwhartoni, T. donaldquickei, T. gracewoodae, T. maetoi, T. montywoodi, T. penteadodiasae, Zacremnops brianbrowni, Z. coatlicue Sharkey, 1990, Zacremnops cressoni (Cameron, 1887), Z. ekchuah Sharkey, 1990, Z. josefernandezi, Zelomorpha sarahmeierottoae. BRACONINAE: Bracon alejandromarini, B. alejandromasisi, B. alexamasisae, B. andresmarini, B. andrewwalshi, B. anniapicadoae, B. anniemoriceae, B. barryhammeli, B. bernardoespinozai, B. carlossanabriai, B. chanchini, B. christophervallei, B. erasmocoronadoi, B. eugeniephillipsae, B. federicomatarritai, B. frankjoycei, B. gerardovegai, B. germanvegai, B. isidrochaconi, B. jimlewisi, B. josejaramilloi, B. juanjoseoviedoi, B. juliodiazi, B. luzmariaromeroae, B. manuelzumbadoi, B. marialuisariasae, B. mariamartachavarriae, B. mariorivasi, B. melissaespinozae, B. nelsonzamorai, B. nicklaphami, B. ninamasisae, B. oliverwalshi, B. paulamarinae, B. rafamoralesi, B. robertofernandezi, B. rogerblancoi, B. ronaldzunigai, B. sigifredomarini, B. tihisiaboshartae, B. wilberthbrizuelai, Digonogastra montylloydi, D. montywoodi, D. motohasegawai, D. natwheelwrighti, D. nickgrishini. CHELONINAE: Adelius adrianguadamuzi, A. gauldi Shimbori & Shaw, 2019, A. janzeni Shimbori & Shaw, 2019, Ascogaster gloriasihezarae, A. grettelvegae, A. guillermopereirai, A. gustavoecheverrii, A. katyvandusenae, A. luisdiegogomezi, Chelonus alejandrozaldivari, C. gustavogutierrezi, C. gustavoinduni, C. harryramirezi, C. hartmanguidoi, C. hazelcambroneroae, C. iangauldi, C. isidrochaconi, C. janecheverriae, C. jeffmilleri, C. jennyphillipsae, C. jeremydewaardi, C. jessiehillae, C. jesusugaldei, C. jimlewisi, C. jimmilleri, C. jimwhitfieldi, C. johanvalerioi, C. johnburnsi, C. johnnoyesi, C. jorgebaltodanoi, C. jorgehernandezi, C. josealfredohernandezi, C. josefernandeztrianai, C. josehernandezcortesi, C. josemanuelperezi, C. josephinerodriguezae, C. juanmatai, C. junkoshimurae, C. kateperezae, C. luciariosae, C. luzmariaromeroae, C. manuelpereirai, C. manuelzumbadoi, C. marianopereirai, C. maribellealvarezae, C. markmetzi, C. markshawi, C. martajimenezae, C. mayrabonillae, C. meganmiltonae, C. melaniamunozae, C. michaelstroudi, C. michellevanderbankae, C. mingfangi, C. minorcarmonai, C. monikaspringerae, C. moniquegilbertae, C. motohasegawai, C. nataliaivanovae, C. nelsonzamorai, C. normwoodleyi, C. osvaldoespinozai, C. pamelacastilloae, C. paulgoldsteini, C. paulhansoni, C. paulheberti, C. petronariosae, C. ramyamanjunathae, C. randallgarciai, C. rebeccakittelae, C. robertoespinozai, C. robertofernandezi, C. rocioecheverriae, C. rodrigogamezi, C. ronaldzunigai, C. rosibelelizondoae, C. rostermoragai, C. ruthfrancoae, C. scottmilleri, C. scottshawi, C. sergioriosi, C. sigifredomarini, C. stevearonsoni, C. stevestroudi, C. sujeevanratnasinghami, C. sureshnaiki, C. torbjornekremi, C. yeimycedenoae, Leptodrepana alexisae, L. erasmocoronadoi, L. felipechavarriai, L. freddyquesadai, L. gilbertfuentesi, L. manuelriosi, Phanerotoma almasolisae, P. alvaroherrerai, P. anacordobae, P. anamariamongeae, P. andydeansi, P. angelagonzalezae, P. angelsolisi, P. barryhammeli, P. bernardoespinozai, P. calixtomoragai, P. carolinacanoae, P. christerhanssoni, P. christhompsoni, P. davesmithi, P. davidduthiei, P. dirksteinkei, P. donquickei, P. duniagarciae, P. duvalierbricenoi, P. eddysanchezi, P. eldarayae, P. eliethcantillanoae, P. jenopappi, Pseudophanerotoma alanflemingi, Ps. albanjimenezi, Ps. alejandromarini, Ps. alexsmithi, Ps. allisonbrownae, Ps. bobrobbinsi. HOMOLOBINAE: Exasticolus jennyphillipsae, E. randallgarciai, E. robertofernandezi, E. sigifredomarini, E. tomlewinsoni. HORMIINAE: Hormius anamariamongeae, H. angelsolisi, H. anniapicadoae, H. arthurchapmani, H. barryhammeli, H. carmenretanae, H. carloswalkeri, H. cesarsuarezi, H. danbrooksi, H. eddysanchezi, H. erikframstadi, H. georgedavisi, H. grettelvegae, H. gustavoinduni, H. hartmanguidoi, H. hectoraritai, H. hesiquiobenitezi, H. irenecanasae, H. isidrochaconi, H. jaygallegosi, H. jimbeachi, H. jimlewisi, H. joelcracrafti, H. johanvalerioi, H. johnburleyi, H. joncoddingtoni, H. jorgecarvajali, H. juanmatai, H. manuelzumbadoi, H. mercedesfosterae, H. modonnellyae, H. nelsonzamorai, H. pamelacastilloae, H. raycypessi, H. ritacolwellae, H. robcolwelli, H. rogerblancosegurai, H. ronaldzunigai, H. russchapmani, H. virginiaferrisae, H. warrenbrighami, H. willsflowersi. ICHNEUTINAE: Oligoneurus kriskrishtalkai, O. jorgejimenezi, Paroligoneurus elainehoaglandae, P. julianhumphriesi, P. mikeiviei. MACROCENTRINAE: Austrozele jorgecampabadali, A. jorgesoberoni, Dolichozele gravitarsis (Muesebeck, 1938), D. josefernandeztrianai, D. josephinerodriguezae, Hymenochaonia kalevikulli, H. kateperezae, H. katherinebaillieae, H. katherineellisonae, H. katyvandusenae, H. kazumifukunagae, H. keithlangdoni, H. keithwillmotti, H. kenjinishidai, H. kimberleysheldonae, H. krisnorvigae, H. lilianamadrigalae, H. lizlangleyae, Macrocentrus fredsingeri, M. geoffbarnardi, M. gregburtoni, M. gretchendailyae, M. grettelvegae, M. gustavogutierrezi, M. hannahjamesae, M. harisridhari, M. hillaryrosnerae, M. hiroshikidonoi, M. iangauldi, M. jennyphillipsae, M. jesseausubeli, M. jessemaysharkae, M. jimwhitfieldi, M. johnbrowni, M. johnburnsi, M. jonathanfranzeni, M. jonathanrosenbergi, M. jorgebaltodanoi, M. lucianocapelli. ORGILINAE: Orgilus amyrossmanae, O. carrolyoonae, O. christhompsoni, O. christinemcmahonae, O. dianalipscombae, O. ebbenielsoni, O. elizabethpennisiae, O. evertlindquisti, O. genestoermeri, O. jamesriegeri, O. jeanmillerae, O. jeffmilleri, O. jerrypowelli, O. jimtiedjei, O. johnlundbergi, O. johnpipolyi, O. jorgellorentei, O. larryspearsi, O. marlinricei, O. mellissaespinozae, O. mikesmithi, O. normplatnicki, O. peterrauchi, O. richardprimacki, O. sandraberriosae, O. sarahmirandae, O. scottmilleri, O. scottmorii, Stantonia billalleni, S. brookejarvisae, S. donwilsoni, S. erikabjorstromae, S. garywolfi, S. henrikekmani, S. luismirandai, S. miriamzunzae, S. quentinwheeleri, S. robinkazmierae, S. ruthtifferae. PROTEROPINAE: Hebichneutes tricolor Sharkey & Wharton, 1994, Proterops iangauldi, P. vickifunkae, Michener charlesi. RHYSIPOLINAE: Pseudorhysipolis luisfonsecai, P. mailyngonzalezaeRhysipolis julioquirosi. ROGADINAE: Aleiodes adrianaradulovae, A. adrianforsythi, A. agnespeelleae, A. alaneaglei, A. alanflemingi, A. alanhalevii, A. alejandromasisi, A. alessandracallejae, A. alexsmithi, A. alfonsopescadori, A. alisundermieri, A. almasolisae, A. alvarougaldei, A. alvaroumanai, A. angelsolisi, A. annhowdenae, A. bobandersoni, A. carolinagodoyae, A. charlieobrieni, A. davefurthi, A. donwhiteheadi, A. doylemckeyi, A. frankhovorei, A. henryhowdeni, A. inga Shimbori & Shaw, 2020, A. johnchemsaki, A. johnkingsolveri, A. gonodontovorus Shimbori & Shaw, 2020, A. manuelzumbadoi, A. mayrabonillae, A. michelledsouzae, A. mikeiviei, A. normwoodleyi, A. pammitchellae, A. pauljohnsoni, A. rosewarnerae, A. steveashei, A. terryerwini, A. willsflowersi, Bioalfa pedroleoni, B. alvarougaldei, B. rodrigogamezi, Choreborogas andydeansi, C. eladiocastroi, C. felipechavarriai, C. frankjoycei, Clinocentrus andywarreni, Cl. angelsolisi, Cystomastax alexhausmanni, Cy. angelagonzalezae, Cy. ayaigarashiae, Hermosomastax clavifemorus Quicke sp. nov., Heterogamus donstonei, Pseudoyelicones bernsweeneyi, Stiropius bencrairi, S. berndkerni, S. edgargutierrezi, S. edwilsoni, S. ehakernae, Triraphis billfreelandi, T. billmclarneyi, T. billripplei, T. bobandersoni, T. bobrobbinsi, T. bradzlotnicki, T. brianbrowni, T. brianlaueri, T. briannestjacquesae, T. camilocamargoi, T. carlosherrerai, T. carolinepalmerae, T. charlesmorrisi, T. chigiybinellae, T. christerhanssoni, T. christhompsoni, T. conniebarlowae, T. craigsimonsi, T. defectus Valerio, 2015, T. danielhubi, T. davidduthiei, T. davidwahli, T. federicomatarritai, T. ferrisjabri, T. mariobozai, T. martindohrni, T. matssegnestami, T. mehrdadhajibabaei, T. ollieflinti, T. tildalauerae, Yelicones dirksteinkei, Y. markmetzi, Y. monserrathvargasae, Y. tricolor Quicke, 1996. Y. woldai Quicke, 1996. The following new combinations are proposed: Neothlipsis smithi (Ashmead), new combination for Microdus smithi Ashmead, 1894; Neothlipsis pygmaeus (Enderlein), new combination for Microdus pygmaeus Enderlein, 1920; Neothlipsis unicinctus (Ashmead), new combination for Microdus unicinctus Ashmead, 1894; Therophilus anomalus (Bortoni and Penteado-Dias) new combination for Plesiocoelus anomalus Bortoni and Penteado-Dias, 2015; Aerophilus areolatus (Bortoni and Penteado-Dias) new combination for Plesiocoelus areolatus Bortoni and Penteado-Dias, 2015; Pneumagathis erythrogastra (Cameron) new combination for Agathis erythrogastra Cameron, 1905. Dolichozele citreitarsis (Enderlein), new combination for Paniscozele citreitarsis Enderlein, 1920. Dolichozele fuscivertex (Enderlein) new combination for Paniscozele fuscivertex Enderlein, 1920. Finally, Bassus brooksi Sharkey, 1998 is synonymized with Agathis erythrogastra Cameron, 1905; Paniscozele griseipes Enderlein, 1920 is synonymized with Dolichozele koebelei Viereck, 1911; Paniscozele carinifrons Enderlein, 1920 is synonymized with Dolichozele fuscivertex (Enderlein, 1920); and Paniscozele nigricauda Enderlein,1920 is synonymized with Dolichozele quaestor (Fabricius, 1804). (originally described as Ophion quaestor Fabricius, 1804).
BackgroundDoubly uniparental inheritance (DUI) is an atypical system of animal mtDNA inheritance found only in some bivalves. Under DUI, maternally (F genome) and paternally (M genome) transmitted mtDNAs yield two distinct gender-associated mtDNA lineages. The oldest distinct M and F genomes are found in freshwater mussels (order Unionoida). Comparative analyses of unionoid mitochondrial genomes and a robust phylogenetic framework are necessary to elucidate the origin, function and molecular evolutionary consequences of DUI. Herein, F and M genomes from three unionoid species, Venustaconcha ellipsiformis, Pyganodon grandis and Quadrula quadrula have been sequenced. Comparative genomic analyses were carried out on these six genomes along with two F and one M unionoid genomes from GenBank (F and M genomes of Inversidens japanensis and F genome of Lampsilis ornata).ResultsCompared to their unionoid F counterparts, the M genomes contain some unique features including a novel localization of the trnH gene, an inversion of the atp8-trnD genes and a unique 3'coding extension of the cytochrome c oxidase subunit II gene. One or more of these unique M genome features could be causally associated with paternal transmission. Unionoid bivalves are characterized by extreme intraspecific sequence divergences between gender-associated mtDNAs with an average of 50% for V. ellipsiformis, 50% for I. japanensis, 51% for P. grandis and 52% for Q. quadrula (uncorrected amino acid p-distances). Phylogenetic analyses of 12 protein-coding genes from 29 bivalve and five outgroup mt genomes robustly indicate bivalve monophyly and the following branching order within the autolamellibranch bivalves: ((Pteriomorphia, Veneroida) Unionoida).ConclusionThe basal nature of the Unionoida within the autolamellibranch bivalves and the previously hypothesized single origin of DUI suggest that (1) DUI arose in the ancestral autolamellibranch bivalve lineage and was subsequently lost in multiple descendant lineages and (2) the mitochondrial genome characteristics observed in unionoid bivalves could more closely resemble the DUI ancestral condition. Descriptions and comparisons presented in this paper are fundamental to a more complete understanding regarding the origins and consequences of DUI.
Here we elucidate and justify a DNA barcode approach to insect species description that can be applied to name tens of thousands of species of Ichneumonoidea and many other species-rich taxa. Each description consists of a lateral habitus image of the specimen, a COI barcode diagnosis, and the holotype specimen information required by the International Code of Zoological Nomenclature. We believe this approach, or a slight modification of it, will be useful for many other underdescribed hyperdiverse taxa, especially in the tropics. Due to the extreme species-richness of the Ichneumonoidea, the very low percentage of described species, and the lack of detailed biological information for most described species, the standard taxonomic approach is inefficient and overwhelmingly time consuming. A DNA barcode-based approach to initial description will provide a solid foundation of species hypotheses from which more comprehensive descriptions can be developed as other data, time, and budgets permit. Here we elucidate this view and detailed methodology that can generally be applied to species-rich underdescribed taxa. A real example is given by describing species in two genera, Hemichoma and Zelomorpha, reared from the Área de Conservación Guanacaste in northwestern Costa Rica. The generic type species Zelomorpha arizonensis is given a DNA barcode diagnosis and the following new species are described: Zelomorpha angelsolisi,
Examinations of breeding system transitions have primarily concentrated on the transition from hermaphroditism to dioecy, likely because of the preponderance of this transition within flowering plants. Fewer studies have considered the reverse transition: dioecy to hermaphroditism. A fruitful approach to studying this latter transition can be sought by studying clades in which transitions between dioecy and hermaphroditism have occurred multiple times. Freshwater crustaceans in the family Limnadiidae comprise dioecious, hermaphroditic and androdioecious (males + hermaphrodites) species, and thus this family represents an excellent model system for the assessment of the evolutionary transitions between these related breeding systems. Herein we report a phylogenetic assessment of breeding system transitions within the family using a total evidence comparative approach. We find that dioecy is the ancestral breeding system for the Limnadiidae and that a minimum of two independent transitions from dioecy to hermaphroditism occurred within this family, leading to (1) a Holarctic, all‐hermaphrodite species, Limnadia lenticularis and (2) mixtures of hermaphrodites and males in the genus Eulimnadia. Both hermaphroditic derivatives are essentially females with only a small amount of energy allocated to male function. Within Eulimnadia, we find several all‐hermaphrodite populations/species that have been independently derived at least twice from androdioecious progenitors within this genus. We discuss two adaptive (based on the notion of ‘reproductive assurance’) and one nonadaptive explanations for the derivation of all‐hermaphroditism from androdioecy. We propose that L. lenticularis likely represents an all‐hermaphrodite species that was derived from an androdioecious ancestor, much like the all‐hermaphrodite populations derived from androdioecy currently observed within the Eulimnadia. Finally, we note that the proposed hypotheses for the dioecy to hermaphroditism transition are unable to explain the derivation of a fully functional, outcrossing hermaphroditic species from a dioecious progenitor.
We provide the first molecular phylogeny of the clerid lineage (Coleoptera: Cleridae, Thanerocleridae) within the superfamily Cleroidea to examine the two most recently proposed hypotheses of higher level classification. Phylogenetic relationships of checkered beetles were inferred from approximately ∼5000 nt of both nuclear and mitochondrial rDNA (28S, 16S and 12S) and the mitochondrial protein‐coding gene COI. A worldwide sample of ∼70 genera representing almost a quarter of generic diversity of the clerid lineage was included and phylogenies were reconstructed using Bayesian and Maximum Likelihood approaches. Results support the monophyly of many proposed subfamilies but were not entirely congruent with either current classification system. The subfamilial relationships within the Cleridae are resolved with support for three main lineages. Tillinae are supported as the sister group to all other subfamilies within the Cleridae, whereas Thaneroclerinae, Korynetinae and a new subfamily formally described here, Epiclininae subf.n., form a sister group to Clerinae + Hydnocerinae.
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