Avian Phylogenomics Project

První strana úvodníku v žurnálu Science, shrnujícího výsledky APP. (Zdroj: Zhang et al. 2014: 1308)

    Před několika hodinami byly napříč 8 různými žurnály prakticky současně publikovány výsledky Avian Phylogenomics Project (APP), výzkumného programu, na kterém se v předchozích čtyřech letech podílelo 80 institucí z celého světa. Výsledkem stovek let procesorového času a nákladů v hodnotě milionů dolarů je 45 nových anotovaných jaderných genomů, tj. plný 15-násobek počtu, který byl k dispozici před rokem, a – ačkoli některé genomy se v literatuře objevily už loni – zhruba 7-násobek toho, co jsme měli ještě včera. Celkem vzato jde dost možná o největší pokrok v ptačí genetice od vynálezu PCR.

    Na APP není zajímavý ani tak objem nashromážděných dat jako spíš praktická ukázka, co vše se s těmito daty dá dělat. Na včerejšek načasovaná lavina studií aplikuje získaná data napříč všemi obory biologie. Kromě bezprecedentně robustního odhadu fylogeneze, tvořícího východisko pro všechny další analýzy, APP odhaluje molekulární základy nejzajímavějších fenotypických novinek jak ptáků coby celku (peří, ztráta zubů, unikátní průtokový dýchací systém s rigidními plícemi), tak i jejich podskupin (tučňáčí adaptace na chlad, vokální učení psittakopasseranů). Genomová evoluce je analyzována na mnoha různých úrovních (od relativního zastoupení GC a poměru synonymních a non-synonymních substitucí přes karyotypovou evoluci až po paleoviry a vznik pohlavních chromozomů) a řada studií vykazuje přesahy do ekologie, diverzifikační dynamiky a ekologie.
    Avian Phylogenomics Project je vnímán jen jako začátek daleko rozsáhlejšího programu, jehož cílem je osekvenovat 10 000 ptačích genomů. Toho by mělo být dosaženo někdy po roce 2020.

Přehled studií (zahrnuje i několik neptačích prací a prací, které byly publikovány již dříve):

http://avian.genomics.cn/en/

http://www.sciencemag.org/content/346/6215/1308/suppl/DC1
http://www.sci-news.com/genetics/...48-bird-species-avian-family-tree-02340.html

Science:

Zhang G, Li C, Li Q, Li B, Larkin DM, Lee C, Storz JF, Antunes A, Greenwold MJ, Meredith RW, Ödeen A, Cui J, Zhou Q, Xu L, Pan H, Wang Z, Jin L, Zhang P, Hu H, Yang W, Hu J, Xiao J, Yang Z, Liu Y, Xie Q, Yu H, Lian J, Wen P, Zhang F, Li H, Zeng Y, Xiong Z, Liu S, Zhou L, Huang Z, An N, Wang J, Zheng Q, Xiong Y, Wang G, Wang B, Wang J, Fan Y, da Fonseca RR, Alfaro-Núñez A, Campos P, Schubert M, Orlando L, Mourier T, Howard J, Ganapathy G, Pfenning A, Whitney O, Rivas MV, Hara E, Smith J, Farre M, Narayan J, Slavov G, Romanov MN, Borges R, Machado JP, Khan I, Springer MS, Gatesy J, Hoffmann FG, Opazo JC, Håstad O, Sawyer RH, Kim H, Kim K, Kim HJ, Cho S, Li N, Huang Y, Bruford MW, Zhan X, Dixon A, Bertelsen MF, Derryberry E, Warren W, Wilson RK, Li S, Ray DA, Green RE, O'Brien SJ, Griffin D, Johnson WE, Haussler D, Ryder OA, Willerslev E, Graves GR, Alström P, Fjeldså J, Mindell DP, Edwards SV, Braun EL, Rahbek C, Burt DW, Houde P, Zhang Y, Yang H, Wang J, Jarvis ED, Gilbert MTP, Wang J 2014 Comparative genomics across modern bird species reveals insights into avian genome evolution and adaptation. Science 346(6215): 1311–20

Birds are the most species-rich class of tetrapod vertebrates and have wide relevance across many research fields. We explored bird macroevolution using full genomes from 48 avian species representing all major extant clades. The avian genome is principally characterized by its constrained size, which predominantly arose because of lineage-specific erosion of repetitive elements, large segmental deletions, and gene loss. Avian genomes furthermore show a remarkably high degree of evolutionary stasis at the levels of nucleotide sequence, gene synteny, and chromosomal structure. Despite this pattern of conservation, we detected many non-neutral evolutionary changes in protein-coding genes and noncoding regions. These analyses reveal that pan-avian genomic diversity covaries with adaptations to different lifestyles and convergent evolution of traits.

Jarvis ED, Mirarab S, Aberer AJ, Li B, Houde P, Li C, Ho SYW, Faircloth BC, Nabholz B, Howard JT, Suh A, Weber CC, Fonseca RRd, Li J, Zhang F, Li H, Zhou L, Narula N, Liu L, Ganapathy G, Boussau B, Bayzid MdS, Zavidovych V, Subramanian S, Gabaldón T, Capella-Gutiérrez S, Huerta-Cepas J, Rekepalli B, Munch K, Schierup M, Lindow B, Warren WC, Ray D, Green RE, Bruford M, Zhan X, Dixon A, Li S, Li N, Huang Y, Derryberry EP, Bertelsen MF, Sheldon FH, Brumfield RT, Mello CV, Lovell PV, Wirthlin M, Schneider MPC, Prosdocimi F, Samaniego JA, Velazquez AMV, Alfaro-Núñez A, Campos PF, Petersen B, Sicheritz-Ponten T, Pas A, Bailey T, Scofield P, Bunce M, Lambert DM, Zhou Q, Perelman R, Driskell AC, Shapiro B, Xiong Z, Zeng Y, Liu S, Li Z, Liu B, Wu K, Xiao J, Yinqi X, Zheng Q, Zhang Y, Yang H, Wang J, Smeds L, Rheindt FE, Braun M, Fjeldså J, Orlando L, Barker K, Jønsson KA, Johnson W, Koepfli KP, O'Brien S, Haussler D, Ryder OA, Rahbek C, Willerslev E, Graves GR, Glenn TC, McCormack J, Burt D, Ellegren H, Alström P, Edwards SW, Stamatakis A, Mindell DP, Cracraft J, Braun EL, Warnow T, Jun W, Gilbert MTP, Zhang G 2014 Whole genome analyses resolve the early branches in the tree of life of modern birds. Science 346(6215): 1320–31

To better determine the history of modern birds, we performed a genome-scale phylogenetic analysis of 48 species representing all orders of Neoaves using phylogenomic methods created to handle genome-scale data. We recovered a highly resolved tree that confirms previously controversial sister or close relationships. We identified the first divergence in Neoaves, two groups we named Passerea and Columbea, representing independent lineages of diverse and convergently evolved land and water bird species. Among Passerea, we infer the common ancestor of core landbirds to have been an apex predator and confirm independent gains of vocal learning. Among Columbea, we identify pigeons and flamingoes as belonging to sister clades. Even with whole genomes, some of the earliest branches in Neoaves proved challenging to resolve, which was best explained by massive protein-coding sequence convergence and high levels of incomplete lineage sorting that occurred during a rapid radiation after the Cretaceous-Paleogene mass extinction event about 66 million years ago.

Nejlepší dostupný odhad ptačí fylogeneze, založený na věrohodnostní analýze 41,8 megabází jaderné DNA (dataset DNA) od 48 ptačích druhů v programu ExaML a následné bayesovské dataci s 39 fosilními kalibracemi v programu MCMCtree. Barvy větví slouží k rozlišení jednotlivých skupin (viz popisky po pravé straně stromu; "Aequornithia" = Aequornithes; "Caprimulgimorphae" = Strisores; "Phoenicopterimorphae" = Mirandornithes); barvy názvů jednotlivých druhů potom zachycují výskyt některých významných znaků: ptáci schopní vokálního učení jsou vyznačeni zeleně, dravci červeně a vodní ptáci modře.
Bootstrapová podpora je rovna 100% pro všechny uzly mimo těch, u kterých je vyznačena. Je vidět, že ne zcela jistými i v celogenomové analýze zůstávají: (1) sesterský vztah dropů a turak; (2) sesterský vztah Otidimorphae (kukačky, turaka, dropi) a Strisores ("lelci" včetně svišťounů); (3) monofylie Cursorimorphae (dlouhokřídlí plus jádro krátkokřídlých), která ale obdržela 100% podporu v některých jiných analýzách; (4) sesterský vztah Cursorimorphae a hoacina; (5) sesterský vztah Phaethontimorphae (kagu, slunatec, faetoni) a Aequornithes (potáplice, trubkonosí, tučňáci, pelikáni, čápi, kormoráni, volavky, ibisové), který ale obdržel 100% v jiných analýzách; (7) sesterský vztah sov a Coraciimorphae (myšáci, kurol, trogoni, "srostloprstí" včetně šplhavců); (8) monofylie Eucavitaves (trogoni, "srostloprstí" včetně šplhavců). Obrovským úspěchem je ale fakt, že nejvyšší možnou podporu obdržela první divergence v rámci Neoaves, nacházející se mezi klady Columbea (potápky, plameňáci, holubi, stepokuři, mesiti) na jedné straně a Passerea (všichni ostatní neoaviani) na straně druhé. Z výskytu jednotlivých ekologií napříč stromem je patrné, že nelze jednoznačně určit, zda byl poslední společný předek Neoaves pozemním nebo vodním ptákem. Šipka na časové ose v dolní části obrázku vyznačuje K/Pg rozhraní (66 Ma); období křídy je vyznačeno šedě. Je patrné, že analýza Jarvise a spol. do křídy klade jen několik málo bazálních divergencí, což je v rozporu s řadou předchozích molekulárních studií – otázkou je, do jaké míry za tímto výsledkem stojí relativně malý počet taxonů. Přerušovaná šedá čára reprezentuje časový horizont 50 Ma (raný eocén), na kterém už existovaly téměř všechny moderní ptačí "řády". Šedé proužky na jednotlivých uzlech vyznačují 95% intervaly kredibility pro příslušné datum divergence.
Ptačí druhy, odshora dolů: zebřička pestrá (Taeniopygia guttata), pěnkavka prostřední (Geospiza fortis), vrána americká (Corvus brachyrhynchos), pipulka zlatokrká (Manacus vitellinus), pokřovník zelený (Acanthisitta chloris), andulka vlnkovaná (Melopsittacus undulatus), nestor kea (Nestor notabilis), sokol stěhovavý (Falco peregrinus), seriema rudozobá (Cariama cristata), vlha núbijská (Merops nubicus), strakapoud osikový (Picoides pubescens), dvojzoborožec nosorožčí (Buceros rhinoceros), trogon horský (Apaloderma vittatum), kurol madagaskarský (Leptosomus discolor), myšák hnědokřídlý (Colius striatus), sova pálená (Tyto alba), orel bělohlavý (Haliaeetus leucocephalus), orel mořský (Haliaeetus albicilla), kondor krocanovitý (Cathartes aura), pelikán kadeřavý (Pelecanus crispus), volavka stříbřitá (Egretta garzetta), ibis čínský (Nipponia nippon), kormorán velký (Phalacrocorax carbo), buřňák lední (Fulmarus glacialis), tučňák kroužkový (Pygoscelia adeliae), tučňák císařský (Aptenodytes forsteri), potáplice malá (Gavia stellata), faeton žlutozobý (Phaethon lepturus), slunatec nádherný (Eurypyga helias), kulík zrzoocasý (Charadrius vociferus), jeřáb královský (Balearica regulorum), hoacin chocholatý (Opisthocomus hoazin), kalypta růžovohlavá (Calypte anna), rorýs ostnitý (Chaetura pelagica), lelek karolinský (Antrostomus carolinensis), drop hřívnatý (Chlamydotis macqueenii), turako červenokorunkatý (Tauraco erythrolophus), kukačka obecná (Cuculus canorus), mesit hnědý (Mesitornis unicolor), stepokur žlutohrdlý (Pterocles gutturalis), holub skalní (Columba livia), plameňák karibský (Phoenicopterus ruber), potápka roháč (Podiceps cristatus), kur domácí (Gallus gallus), krocan domácí (Meleagris gallopavo), kachna divoká (Anas platyrhynchos), tinama tečkovaná (Tinamus guttatus), pštros dvouprstý (Struthio camelus).
(Zdroj: Jarvis et al. 2014: Supplementary Materials: Figure S1)

Xu X, Zhou Z-H, Dudley R, Mackem S, Chuong C-M, Erickson GM, Varricchio DJ 2014 An integrative approach to understanding bird origins. Science 346 (6215): 1341 (Summary) + 1253293

Background:

The origin of birds is one of the most enduring and dramatic evolutionary debates. The hypothesis that the primarily small-sized birds are nested within a theropod dinosaur group that includes the gigantic Tyrannosaurus rex has been supported by strong fossil evidence, but until recently, several important issues remained unresolved, including the origins of feathers and flight, the “temporal paradox” (the coelurosaurian theropods occur too late in the fossil record to be ancestral to the Jurassic bird Archaeopteryx), and supposed homological incongruities (e.g., the suggested homologies of three fingers in tetanuran theropods are different from those of living birds). Recent discoveries of spectacular dinosaur fossils from China and elsewhere provide new information to address these issues.

Advances:

The discoveries of feathered dinosaur fossils from the Jurassic and Cretaceous sediments of China and elsewhere document a diverse range of feathers from monofilamentous feathers to highly complex flight feathers, which show a general evolutionary trend of increasing complexity leading to the cladogenesis of birds. The wide occurrence of foot feathers in Mesozoic theropods (i.e., short filamentous forms in relatively basal theropods and large vaned forms in derived theropods, including early birds) clarifies feather-scale relations and integumentary evolution pertinent to flight origins and also shows that bird flight likely evolved through a four-winged stage. With numerous discoveries of well-preserved dinosaur fossils over a wide range of geological periods, the morphological, functional, and temporal transition from ground-living to flight-capable theropod dinosaurs is now one of the best-documented major evolutionary transitions. Meanwhile, studies in disciplines other than paleontology provide new insights into how bird characteristics originated and evolved—such as feathers, flight, endothermic physiology, unique strategies for reproduction and growth, and an unusual pulmonary system. The iconic features of extant birds, for the most part, evolved in a gradual and stepwise fashion throughout theropod evolution. However, new data highlight occasional bursts of morphological novelty at certain stages close to the origin of birds and an unavoidable complex, mosaic evolutionary distribution of major bird characteristics on the theropod tree. Research into bird origins provides a model of how an integration of paleontological and neontological data can be used to gain a comprehensive understanding of the complexity surrounding major evolutionary transitions and to set new research directions.

Outlook:

 A refined, more robust phylogeny will be imperative to move our studies forward. A larger data set will help to increase the accuracy of phylogenetic reconstructions, but better character formulation and more accurate scorings are imperative at the current stage. In terms of character evolution, an integrative approach combining paleontological, neontological, developmental, temporal, and even paleoenvironmental data is particularly desirable. Greater examination of fossils pertaining to molecular information is also a potentially fruitful avenue for future investigation. Evolutionary scenarios for various aspects of the origin of birds have sometimes been constructed from neontological data, but any historical reconstruction must ultimately be tested using the fossil record. Consequently, dense fossil sampling along the line to modern birds and better understanding of transitional forms play key roles in such reconstructions.

Nejlepší shrnutí evoluce ptáků v jediném obrázku všech dob. Vybrané druhy archosauromorfů jsou zakresleny na časově kalibrované konsenzuální fylogenezi, jejíž topologie pro bazální teropody vychází z Rauhut et al. (2012) a topologie pro celurosaury z Turner et al. (2012). Výčty znaků u jednotlivých uzlů ukazují, v kterém místě ptačí kmenové linie (stem lineage) vznikly podle současných paleontologických poznatků klíčové evoluční novinky odlišující moderní ptáky od ostatních žijících zvířat. Stáří zobrazených taxonů ukazuje, že tzv. "temporal paradox", kterým v minulosti argumentovali odpůrci dinosauřího původu ptáků, neexistuje: známe řadu celurosaurů starších než Archaeopteryx (včetně zástupců ptačí sesterské skupiny) a stratigrafický výskyt obecně velmi dobře koresponduje s fylogenetickou pozicí (bazálnější taxony jsou starší než ty odvozené). Kosterní siluety po pravé straně ilustrují změny v celkové morfologii na vývojové linii vedoucí k ptákům. Odspoda nahoru: raný archosauriform Euparkeria, raný krokodylomorf Sphenosuchus, raný teropod Coelophysis, raný celurosaur (snad bazální tyrannosauroid) Proceratosaurus, raní paraviani Anchiornis (snad bazální avialan nebo troodontid) a Archaeopteryx (snad bazální avialan nebo bazální deinonychosaur), raný krátkoocasý pták Sapeornis, raný ornituromorf Yanornis, moderní pták Columba (holub).

Zkratky (od spodních uzlů k horním): (UB) průtoková dýchací soustava, (BMR) bazální metabolický výdej, (GR) rychlost růstu, (FF) vláknité peří, (SP) pneumatizace kostí, (BL) pohyb po dvou nohou, (CASPE) krční vzdušné vaky rozšířené směrem dozadu, (TFH) tříprstá ruka, (LFC) schopnost složit přední končetinu přitažením záprstí k předloktí, (KBL) pohyb založený na ohýbání kolene místo kyčle, (CCIASE) diferenciace klíčkového vzdušného vaku a břišních vzdušných vaků, (ES) velikost vajec, (VF) obrysová pera, (CE) zvětšení mozku v poměru k tělu, (AFC) schopnost mávavého pohybu předními končetinami, (PPO) obrácení stydké kosti dozadu, (SBT) krátký kostěný ocas, (ACVP) pokročilá kostosternální pumpa – plicní ventilace zajišťována rozpínáním a stlačováním hrudi pomocí svalů upínajících se na hrudní kost a žebra, (SAE) lehce asymetrická vejce, (MO) monoautochronní ovulace – v každém ovulačním cyklu uvolněno z obou vaječníků synchronizovaně právě jedno vajíčko, (IL) vejce snášená v denních nebo několikadenních intervalech, (PC) samčí péče o mláďata, (AL) pohyb vzduchem, (EM) extrémní miniaturizace, (AET) prodloužení a zesílení přední končetiny, (VABRE) rozvoj částí mozků spojených se zrakem, (IA) zvýšená asymetrie, (US) povrch skořápky bez ornamentace, (LP) nízká porozita, (TL) třetí (vnější) vrstva, (ICI) sezení na vejcích, (FPB) srůst pánevních kostí, (RLP) tyčkovitý pygostyl, (AOO) aktivní vaječník a vejcovod, (KS) kinetická lebka, (PSP) radlicovitý pygostyl, (RMILTAY) rychlé dosažení dospělosti v prvním roce života, (ECFSC) snůška vajec nepřikrytá sedimentem, (ER) otáčení vajec

Znaky související s evolucí vzdušných vaků (CASPE, CCIASE, ACVP) se zdají být založeny na kontroverzní studii Serena a spol. (2008); viz proto kritické poznámky Matta Wedela. Nejisté jsou i fylogenetické vztahy na bázi Paraves – více v tomto článku.

(Zdroj: Xu et al. 2014: Figure 2)

Mirarab S, Bayzid MdS, Boussau B, Warnow T 2014 Statistical binning enables an accurate coalescent-based estimation of the avian tree. Science 346(6215): 1337 (Summary) + 1250463

http://www.sciencemag.org/content/346/6215/1250463.abstract

Introduction:

Reconstructing species trees for rapid radiations, as in the early diversification of birds, is complicated by biological processes such as incomplete lineage sorting (ILS) that can cause different parts of the genome to have different evolutionary histories. Statistical methods, based on the multispecies coalescent model and that combine gene trees, can be highly accurate even in the presence of massive ILS; however, these methods can produce species trees that are topologically far from the species tree when estimated gene trees have error. We have developed a statistical binning technique to address gene tree estimation error and have explored its use in genomescale species tree estimation with MP-EST, a popular coalescent-based species tree estimation method.

Rationale:

In statistical binning, phylogenetic trees on different genes are estimated and then placed into bins, so that the differences between trees in the same bin can be explained by estimation error (see the figure). A new tree is then estimated for each bin by applying maximum likelihood to a concatenated alignment of the multiple sequence alignments of its genes, and a species tree is estimated using a coalescent-based species tree method from these supergene trees.

Results:

Under realistic conditions in our simulation study, statistical binning reduced the topological error of species trees estimated using MP-EST and enabled a coalescent-based analysis that was more accurate than concatenation even when gene tree estimation error was relatively high. Statistical binning also reduced the error in gene tree topology and species tree branch length estimation, especially when the phylogenetic signal in gene sequence alignments was low. Species trees estimated using MP-EST with statistical binning on four biological data sets showed increased concordance with the biological literature. When MP-EST was used to analyze 14,446 gene trees in the avian phylogenomics project, it produced a species tree that was discordant with the concatenation analysis and conflicted with prior literature. However, the statistical binning analysis produced a tree that was highly congruent with the concatenation analysis and was consistent with the prior scientific literature.

Conclusions:

Statistical binning reduces the error in species tree topology and branch length estimation because it reduces gene tree estimation error. These improvements are greatest when gene trees have reduced bootstrap support, which was the case for the avian phylogenomics project. Because using unbinned gene trees can result in overestimation of ILS, statistical binning may be helpful in providing more accurate estimations of ILS levels in biological data sets. Thus, statistical binning enables highly accurate species tree estimations, even on genome-scale data sets. 

Meredith RW, Zhang G, Gilbert MTP, Jarvis ED, Springer MS 2014 Evidence for a single loss of mineralized teeth in the common avian ancestor. Science 346(6215): 1336 (Summary) + 1254390

Introduction:

The absence of teeth or edentulism has evolved on multiple occasions within vertebrates, including birds, turtles, and a few groups of mammals (anteaters, baleen whales, and pangolins). There are also mammals with enamelless teeth (aardvarks, sloths, and armadillos). All toothless/enamelless vertebrates are descended from ancestors with enamelcapped teeth. In the case of birds, it is theropod dinosaurs. Instead of teeth, modern birds use a horny beak (rhamphotheca) and part of their digestive tract (muscular gizzard) to grind up and process food. The fossil record of early birds is fragmentary, and it is unclear whether tooth loss evolved in the common ancestor of all modern birds or convergently in two or more independent lineages.

Rationale:

Tooth formation in vertebrates is a complicated process that involves many different genes. Of these genes, six are essential for the proper formation of dentin (DSPP) and enamel (AMTN, AMBN, ENAM, AMELX, and MMP20). We examined these six genes in the genomes of 48 bird species, which represent nearly all living bird orders, as well as the American alligator, a representative of Crocodylia (the closest living relatives of birds), for the presence of inactivating mutations that are shared by all 48 birds. The presence of such shared mutations in dentin and enamel-related genes would suggest a single loss of mineralized teeth in the common ancestor of all living birds. We also queried the genomes of additional toothless/enamelless vertebrates, including three turtles and four mammals, for inactivating mutations in these genes. For comparison, we looked at the genomes of mammalian taxa with enamel-capped teeth.

Results:

All edentulous vertebrate genomes that were examined are characterized by inactivating mutations in DSPP, AMBN, AMELX, AMTN, ENAM, and MMP20, rendering these genes nonfunctional. The dentin-related gene DSPP is functional in vertebrates with enamelless teeth (sloth, aardvark, and armadillo). All six genes are functional in the American alligator and mammalian taxa with enamelcapped teeth. More important, 48 bird species share inactivating mutations in both dentin-related (DSPP) and enamel-related genes (ENAM, AMELX, AMTN, and MMP20), indicating that the genetic machinery necessary for tooth formation was lost in the common ancestor of all modern birds. Furthermore, the frameshift mutation rate in birds suggests that the outer enamel covering of teeth was lost about 116 million years ago.

Conclusions:

We postulate, on the basis of fossil and molecular evidence, a two-step scenario whereby tooth loss and beak development evolved together in the common ancestor of all modern birds. In the first stage, tooth loss and partial beak development commenced on the anterior portion of both the upper and lower jaws. The second stage involved concurrent progression of tooth loss and beak development from the anterior portion of both jaws to the back of the rostrum. We propose that this progression ultimately resulted in a complete horny beak that effectively replaced the teeth and may have contributed to the diversification of living birds.

Green RE, Braun EL, Armstrong J, Earl D, Nguyen N, Hickey G, Vandewege MW, St. John JA, Capella-Gutiérrez S, Castoe TA, Kern C, Fujita MK, Opazo JC, Jurka J, Kojima KK, Caballero J, Hubley RM, Smit AF, Platt RN, Lavoie CA, Ramakodi MP, Finger Jr JW, Suh A, Isberg SR, Miles L, Chong AY, Jaratlerdsiri W, Gongora J, Moran C, Iriarte A, McCormack J, Burgess SC, Edwards SV, Lyons E, Williams C, Breen M, Howard JT, Gresham CR, Peterson DG, Schmitz J, Pollock DD, Haussler D, Triplett EW, Zhang G, Irie N, Jarvis ED, Brochu CA, Schmidt CJ, McCarthy FM, Faircloth BG, Hoffmann FG, Glenn TC, Gabaldón T, Paten B, Ray DA 2014 Three crocodilian genomes reveal ancestral patterns of evolution among archosaurs. Science 346(6215): 1335 (Summary) + 1254449

Introduction:

Crocodilians and birds are the two extant clades of archosaurs, a group that includes the extinct dinosaurs and pterosaurs. Fossils suggest that living crocodilians (alligators, crocodiles, and gharials) have a most recent common ancestor 80 to 100 million years ago. Extant crocodilians are notable for their distinct morphology, limited intraspecific variation, and slow karyotype evolution. Despite their unique biology and phylogenetic position, little is known about genome evolution within crocodilians.

Rationale:

Genome sequences for the American alligator, saltwater crocodile, and Indian gharial—representatives of all three extant crocodilian families—were obtained to facilitate better understanding of the unique biology of this group and provide a context for studying avian genome evolution. Sequence data from these three crocodilians and birds also allow reconstruction of the ancestral archosaurian genome.

Results:

We sequenced shotgun genomic libraries from each species and used a variety of assembly strategies to obtain draft genomes for these three crocodilians. The assembled scaffold N50 was highest for the alligator (508 kilobases). Using a panel of reptile genome sequences, we generated phylogenies that confirm the sister relationship between crocodiles and gharials, the relationship with birds as members of extant Archosauria, and the outgroup status of turtles relative to birds and crocodilians. We also estimated evolutionary rates along branches of the tetrapod phylogeny using two approaches: ultraconserved element–anchored sequences and fourfold degenerate sites within stringently filtered orthologous gene alignments. Both analyses indicate that the rates of base substitution along the crocodilian and turtle lineages are extremely low. Supporting observations were made for transposable element content and for gene family evolution. Analysis of whole-genome alignments across a panel of reptiles and mammals showed that the rate of accumulation of microinsertions and microdeletions is proportionally lower in crocodilians, consistent with a single underlying cause of a reduced rate of evolutionary change rather than intrinsic differences in base-repair machinery. We hypothesize that this single cause may be a consistently longer generation time over the evolutionary history of Crocodylia. Low heterozygosity was observed in each genome, consistent with previous analyses, including the Chinese alligator. Pairwise sequential Markov chain analysis of regional heterozygosity indicates that during glacial cycles of the Pleistocene, each species suffered reductions in effective population size. The reduction was especially strong for the American alligator, whose current range extends farthest into regions of temperate climates.

Conclusion:

We used crocodilian, avian, and outgroup genomes to reconstruct 584 megabases of the archosaurian common ancestor genome and the genomes of key ancestral nodes. The estimated accuracy of the archosaurian genome reconstruction is 91% and is higher for conserved regions such as genes. The reconstructed genome can be improved by adding more crocodilian and avian genome assemblies and may provide a unique window to the genomes of extinct organisms such as dinosaurs and pterosaurs. 

Whitney O, Pfenning AR, Howard JT, Blatti CA, Liu F,  Ward JM, Wang R, Audet J-N, Kellis M, Mukherjee S, Sinha S, Hartemink AJ, West AE, Jarvis ED 2014 Core and region-enriched networks of behaviorally regulated genes and the singing genome. Science 346(6215): 1334 (Summary) + 1256780

Introduction:

Brain activity drives both behavior and regulated gene expression in neurons. Although past studies have identified activity-induced signaling and gene regulation cascades in cultured neurons, much less is known about how activity-dependent transcriptional networks are affected by the variations in cell-type composition, network interconnections, and firing patterns that comprise behaviorally active brain circuits in vivo.

Rationale:

We tested the hypothesis that behaviorally regulated gene expression is anatomically and temporally diverse and that the key determinants of this diversity are networks of transcription factors, their genomic binding sites, and epigenetic chromatin states. We analyzed genome-wide, singingregulated gene expression across time in the four major forebrain regions of the song control system in songbirds, a model of speech production in humans. We then performed a transcription factor motif analysis to identify gene regulatory networks enriched in each song nucleus and measured acetylation of histone 3 at lysine 27 (H3K27ac) to identify chromatin regions that were transcriptionally active in the genomes of song nuclei before and after singing.

Results:

We found that singing was associated with differential regulation of about 10% of all genes in the avian genome that came in several waves across time. Less than 1% of these genes were comparably regulated in all song nuclei tested, and these comprised a core set dominated by immediate-early gene (IEG) transcription factors. By contrast, the vast majority of singing-regulated genes were regulated in only one or a subset of song nuclei, such that each song nucleus had its own dominant subset of genes regulated with defined temporal profiles, controlling a variety of functions. The promoters of many of the singing-regulated genes contained binding motifs for known early-activated transcription factors (EATFs) that become active in response to neural firing, some of which were expressed differentially between song nuclei at baseline. One EATF, calciumresponse factor (CaRF), was tested with RNA interference knockdown in cultured neurons and found to regulate the predicted genes in response to neural activity, but was also found to modulate their expression even at baseline. More strikingly, we found with H3K27ac analysis that many song nucleus–specific singing-regulated genes did not show increased chromatin regulatory element activity after singing but rather already had primed region-specific regulatory activity before singing began.

Conclusions:

We propose a dual mechanism for the diversity of behaviorally regulated genes across different brain regions in vivo (see the figure). First, the neural activity associated with singing activates EATFs, and some TFs differentially expressed in brain regions at baseline, to trigger region-specific expression of their target genes. Second, brain region–specific enhancers near activity-regulated genes are waiting in an epigenetically primed state, ready to modulate transcription of general and song nucleus– specific genes at a moment’s notice when the neurons fire. The combination of these two mechanisms underlies a great diversity of behaviorally regulated gene expression, permitting each nucleus to perform its particular function in this complex behavior.

Pfenning AR, Hara E, Whitney O, Rivas MV, Wang R, Roulhac PL, Howard JT, Wirthlin M, Lovell PV, Ganapathy G, Mouncastle J, Moseley MA, Thompson JW, Soderblom EJ, Iriki A, Kato M, Gilbert MTP, Zhang G, Bakken T, Bongaarts A, Bernard A, Lein E, Mello CV, Hartemink AJ, Jarvis ED 2014 Convergent transcriptional specializations in the brains of humans and song-learning birds. Science 346(6215): 1333 (Summary) + 1256846

Introduction:

Vocal learning, the ability to imitate sounds, is a trait that has undergone convergent evolution in several lineages of birds and mammals, including song-learning birds and humans. This behavior requires cortical and striatal vocal brain regions, which form unique connections in vocal-learning species. These regions have been found to have specialized gene expression within some species, but the patterns of specialization across vocallearning bird and mammal species have not been systematically explored.

Rationale:

The sequencing of genomes representing all major vocal-learning and vocal-nonlearning avian lineages has allowed us to develop the genomic tools to measure anatomical gene expression across species. Here, we asked whether behavioral and anatomical convergence is associated with gene expression convergence in the brains of vocal-learning birds and humans.

Results:

We developed a computational approach that discovers homologous and convergent specialized anatomical gene expression profiles. This includes generating hierarchically organized gene expression specialization trees for each species and a dynamic programming algorithm that finds the optimal alignment between species brain trees. We applied this approach to brain region gene expression databases of thousands of samples and genes that we and others generated from multiple species, including humans and song-learning birds (songbird, parrot, and hummingbird) as well as vocalnonlearning nonhuman primates (macaque) and birds (dove and quail). Our results confirmed the recently revised understanding of the relationships between avian and mammalian brains. We further found that songbird Area X, a striatal region necessary for vocal learning, was most similar to a part of the human striatum activated during speech production. The RA (robust nucleus of the arcopallium) analog of song-learning birds, necessary for song production, was most similar to laryngeal motor cortex regions in humans that control speech production. More than 50 genes contributed to their convergent specialization and were enriched in motor control and neural connectivity functions. These patterns were not found in vocal nonlearners, but songbird RA was similar to layer 5 of primate motor cortex for another set of genes, supporting previous hypotheses about the similarity of these cell types between bird and mammal brains.

Conclusion:

Our approach can accurately and quantitatively identify functionally and molecularly analogous brain regions between species separated by as much as 310 million years from a common ancestor. We were able to identify analogous brain regions for song and speech between birds and humans, and broader homologous brain regions in which these specialized song and speech regions are located, for tens to hundreds of genes. These genes now serve as candidates involved in developing and maintaining the unique connectivity and functional properties of vocal-learning brain circuits shared across species. The finding that convergent neural circuits for vocal learning are accompanied by convergent molecular changes of multiple genes in species separated by millions of years from a common ancestor indicates that brain circuits for complex traits may have limited ways in which they could have evolved from that ancestor.

Zhou Q, Zhang J, Bachtrog D, An N, Huang Q, Jarvis ED, Gilbert MTP, Zhang G 2014 Complex evolutionary trajectories of sex chromosomes across bird taxa. Science 346(6215): 1332 (Summary) + 1246338

Introduction:

Sex chromosomes originate from ordinary autosomes. Ancient sexspecific W or Y chromosomes, like that of female chicken or those of male mammals, usually have lost most functional genes, owing to a loss of recombination with their former homologs, the Z or X chromosomes. Such a recombination restriction occurred in a stepwise manner along most of the sex chromosomes in parallel in birds and mammals (creating so-called “evolutionary strata”), apart from small pseudoautosomal regions (PARs) that maintain recombination. Sex chromosomes of some basal birds like ostrich and emu have exceptionally large recombining PARs, but little is known about the genomic composition of most bird species’ sex chromosomes.

Rationale:

Here we use the newly available genomes of 17 species spanning the entire avian phylogeny to decipher the genomic architecture and evolutionary history of bird sex chromosomes. We demarcate the PAR and the nonrecombining differentiated region between Z/W of each species by their different read depths relative to autosomes. We further assemble numerous W-linked genomic regions, whose abundance and sequence divergence level with Z chromosome reflect their ages of recombination loss.

Results:

Surprisingly, we find that more than half of the studied species have a W chromosome that is not completely degenerated. Besides ostrich and emu, some Neognathae species like tropicbird and killdeer also have long PARs. The nonrecombining regions between Z/W of many species exhibit a complex pattern of “evolutionary strata,” resulting from the suppression of recombination in a stepwise and independent manner among some lineages. We conclude that the first evolutionary stratum that contains the putative male-determining gene DMRT1 formed through a Z-linked chromosome inversion in an ancestor of all birds. This was followed by one stratum formed in the ancestor of Neognathae, one stratum in the ancestor of Neoaves, and independent emergence of more recent strata in most species. Many W-linked genes have disrupted protein function or reduced gene expression, and the rate of functional decay significantly slows down in older strata.

Conclusion:

Our study uncovered an unexpected complexity of avian sex chromosomes, due to the lineage-specific recombination suppressions and different tempo of W degeneration. In contrast to mammals, some birds never experienced global recombination arrest, or differentiate at a very low rate between Z/W even after the recombination loss. This may relate to different intensities of sexual selection across bird species and explain their lack of a general chromosome-wide dosage compensation mechanism.

Úvodníky, populárně-naučné shrnutí:

Zhang G, Jarvis ED, Gilbert MTP A flock of genomes. Science 346(6215): 1308–9

Kress WJ 2014 Valuing collections. Science 346(6215): 1310

http://www.sciencemag.org/content/346/6215/1310

This year brought dismal news about the world's birds: They are vanishing at an alarming rate. Across 25 European countries, about 420 million fewer birds are present today than in 1980, a 20% decrease, especially in the 36 most common species. In North America, The State of the Birds Report 2014 indicates that over the past 40 years, the numbers of individuals across 33 species are also down by hundreds of millions. Such assessments highlight the urgency of determining the precise causes of these declines. The knowledge gleaned from the Avian Phylogenomics Project, coupled with ecological and population analyses, should provide new insights into the factors that influence bird declines and extinctions. As the project progresses over the next few years, over 60% of tissue samples for the avian analyses will be derived from archived museum collections. In this era of deteriorating natural environments, a pressing challenge is to continue to build scientific collections for future needs.

Pennisi E 2014 Bird genomes give new perches to old friends. Science 346(6215): 1275–6

The placement of a strange South American bird called the hoatzin in the avian family tree is one of the many findings revealed this week from a massive international project analyzing the sequenced genomes of 48 bird species representing nearly every order of bird. The effort, involving 200 people from 80 labs and weeks of supercomputer time, has yielded the most definitive avian family tree yet. It has also pinpointed gene networks underlying the traits that make birds birds, such as feathers and beaks instead of teeth. In one provocative finding, a team has identified the gene network that underlies complex singing in birds—and found that the same network operates in humans, where it is presumably crucial to language. Already, 200 more bird genomes have been sequenced, with more waiting in the wings.

Genome Biology:

Cui J, Zhao W, Huang Z, Jarvis ED, Gilbert MTP, Walker PJ, Holmes EC, Zhang G 2014 Low frequency of paleoviral infiltration across the avian phylogeny. Genome Biol 15: 539

Background:

Mammalian genomes commonly harbor endogenous viral elements. Due to a lack of comparable genome-scale sequence data, far less is known about endogenous viral elements in avian species, even though their small genomes may enable important insights into the patterns and processes of endogenous viral element evolution.

Results:

Through a systematic screening of the genomes of 48 species sampled across the avian phylogeny we reveal that birds harbor a limited number of endogenous viral elements compared to mammals, with only five viral families observed: Retroviridae, Hepadnaviridae, Bornaviridae, Circoviridae, and Parvoviridae. All nonretroviral endogenous viral elements are present at low copy numbers and in few species, with only endogenous hepadnaviruses widely distributed, although these have been purged in some cases. We also provide the first evidence for endogenous bornaviruses and circoviruses in avian genomes, although at very low copy numbers. A comparative analysis of vertebrate genomes revealed a simple linear relationship between endogenous viral element abundance and host genome size, such that the occurrence of endogenous viral elements in bird genomes is 6- to 13-fold less frequent than in mammals.

Conclusions:

These results reveal that avian genomes harbor relatively small numbers of endogenous viruses, particularly those derived from RNA viruses, and hence are either less susceptible to viral invasions or purge them more effectively.

Weber CC, Nabholz B, Romiguier J, Ellegren H 2014 K_r/K_c but not d_N/d_S correlates positively with body mass in birds, raising implications for inferring lineage-specific selection. Genome Biol 15: 542

Background:

The ratio of the rates of non-synonymous and synonymous substitution (d_N/d_S) is commonly used to estimate selection in coding sequences. It is often suggested that, all else being equal, d_N/d_S should be lower in populations with large effective size (N_e) due to increased efficacy of purifying selection. As N_e is difficult to measure directly, life history traits such as body mass, which is typically negatively associated with population size, have commonly been used as proxies in empirical tests of this hypothesis. However, evidence of whether the expected positive correlation between body mass and d_N/d_S is consistently observed is conflicting.

Results:

Employing whole genome sequence data from 48 avian species, we assess the relationship between rates of molecular evolution and life history in birds. We find a negative correlation between d_N/d_S and body mass, contrary to nearly neutral expectation. This raises the question whether the correlation might be a method artefact. We therefore in turn consider non-stationary base composition, divergence time and saturation as possible explanations, but find no clear patterns. However, in striking contrast to d_N/d_S, the ratio of radical to conservative amino acid substitutions (K_r/K_c) correlates positively with body mass.

Conclusions:

Our results in principle accord with the notion that non-synonymous substitutions causing radical amino acid changes are more efficiently removed by selection in large populations, consistent with nearly neutral theory. These findings have implications for the use of d_N/d_S and suggest that caution is warranted when drawing conclusions about lineage-specific modes of protein evolution using this metric.

Weber CC, Boussau B, Romiguier J, Jarvis ED, Ellegren H 2014 Evidence for GC-biased gene conversion as a driver of between-lineage differences in avian base composition. Genome Biol 15: 549

Background:

While effective population size (N_e) and life history traits such as generation time are known to impact substitution rates, their potential effects on base composition evolution are less well understood. GC content increases with decreasing body mass in mammals, consistent with recombination-associated GC biased gene conversion (gBGC) more strongly impacting these lineages. However, shifts in chromosomal architecture and recombination landscapes between species may complicate the interpretation of these results. In birds, interchromosomal rearrangements are rare and the recombination landscape is conserved, suggesting that this group is well suited to assess the impact of life history on base composition.

Results:

Employing data from 45 newly and 3 previously sequenced avian genomes covering a broad range of taxa, we found that lineages with large populations and short generations exhibit higher GC content. The effect extends to both coding and non-coding sites, indicating that it is not due to selection on codon usage. Consistent with recombination driving base composition, GC content and heterogeneity were positively correlated with the rate of recombination. Moreover, we observed ongoing increases in GC in the majority of lineages.

Conclusions:

Our results provide evidence that gBGC may drive patterns of nucleotide composition in avian genomes and are consistent with more effective gBGC in large populations and a greater number of meioses per unit time; that is, a shorter generation time. Thus, in accord with theoretical predictions, base composition evolution is substantially modulated by species life history.

Li S, Li B, Cheng C, Xiong Z, Liu Q, Lai J, Carey HV, Zhang Q, Zheng H, Wei S, Zhang H, Chang L, Liu S, Zhang S, Yu B, Zeng X, Hou Y, Nie W, Guo Y, Chen T, Han J, Wang J, Wang J, Chen C, Liu J, Stambrook PJ, Xu M, Zhang G, Gilbert MTP, Yang H, Jarvis ED, Yu J, Yan J 2014 Genomic signatures of near-extinction and rebirth of the crested ibis and other endangered bird species. Genome Biol 15: 557

Background:

Nearly a quarter of all avian species is either threatened or nearly threatened. Of these, 73 species are currently being rescued from going extinct in wildlife sanctuaries. One of the previously most critically-endangered is the crested ibis, Nipponia nippon. Once widespread across North-East Asia, by 1981 only seven individuals from two breeding pairs remained in the wild. The recovering crested ibis populations thus provide an excellent example for conservation genomics since every individual bird has been recruited for genomic and demographic studies.

Results:

Using high-quality genome sequences of multiple crested ibis individuals, its thriving co-habitant, the little egret, Egretta garzetta, and the recently sequenced genomes of 41 other avian species that are under various degrees of survival threats, including the bald eagle, we carry out comparative analyses for genomic signatures of near extinction events in association with environmental and behavioral attributes of species. We confirm that both loss of genetic diversity and enrichment of deleterious mutations of protein-coding genes contribute to the major genetic defects of the endangered species. We further identify that genetic inbreeding and loss-of-function genes in the crested ibis may all constitute genetic susceptibility to other factors including long-term climate change, over-hunting, and agrochemical overuse. We also establish a genome-wide DNA identification platform for molecular breeding and conservation practices, to facilitate sustainable recovery of endangered species.

Conclusions:

These findings demonstrate common genomic signatures of population decline across avian species and pave a way for further effort in saving endangered species and enhancing conservation genomic efforts.

Lovell PV, Wirthlin M, Wilhelm L, Minx P, Lazar NH, Carbone L, Warren WC, Mello CV 2014 Conserved syntenic clusters of protein coding genes are missing in birds. Genome Biol 15: 565 

Background:

Birds are one of the most highly successful and diverse groups of vertebrates, having evolved a number of distinct characteristics, including feathers and wings, a sturdy lightweight skeleton and unique respiratory and urinary/excretion systems. However, the genetic basis of these traits is poorly understood.

Results:

Using comparative genomics based on extensive searches of 60 avian genomes, we have found that birds lack approximately 274 protein coding genes that are present in the genomes of most vertebrate lineages and are for the most part organized in conserved syntenic clusters in non-avian sauropsids and in humans. These genes are located in regions associated with chromosomal rearrangements, and are largely present in crocodiles, suggesting that their loss occurred subsequent to the split of dinosaurs/birds from crocodilians. Many of these genes are associated with lethality in rodents, human genetic disorders, or biological functions targeting various tissues. Functional enrichment analysis combined with orthogroup analysis and paralog searches revealed enrichments that were shared by non-avian species, present only in birds, or shared between all species.

Conclusions:

Together these results provide a clearer definition of the genetic background of extant birds, extend the findings of previous studies on missing avian genes, and provide clues about molecular events that shaped avian evolution. They also have implications for fields that largely benefit from avian studies, including development, immune system, oncogenesis, and brain function and cognition. With regards to the missing genes, birds can be considered ‘natural knockouts’ that may become invaluable model organisms for several human diseases.

GigaScience:

Zhang G, Li B, Li C, Gilbert MTP, Jarvis ED, Wang J, The Avian Genome Consortium 2014 Comparative genomic data of the Avian Phylogenomics Project. GigaScience 3: 26

Background:

The evolutionary relationships of modern birds are among the most challenging to understand in systematic biology and have been debated for centuries. To address this challenge, we assembled or collected the genomes of 48 avian species spanning most orders of birds, including all Neognathae and two of the five Palaeognathae orders, and used the genomes to construct a genome-scale avian phylogenetic tree and perform comparative genomics analyses (Jarvis et al. in press; Zhang et al. in press). Here we release assemblies and datasets associated with the comparative genome analyses, which include 38 newly sequenced avian genomes plus previously released or simultaneously released genomes of Chicken, Zebra finch, Turkey, Pigeon, Peregrine falcon, Duck, Budgerigar, Adelie penguin, Emperor penguin and the Medium Ground Finch. We hope that this resource will serve future efforts in phylogenomics and comparative genomics.

Findings:

The 38 bird genomes were sequenced using the Illumina HiSeq 2000 platform and assembled using a whole genome shotgun strategy. The 48 genomes were categorized into two groups according to the N50 scaffold size of the assemblies: a high depth group comprising 23 species sequenced at high coverage (>50X) with multiple insert size libraries resulting in N50 scaffold sizes greater than 1 Mb (except the White-throated Tinamou and Bald Eagle); and a low depth group comprising 25 species sequenced at a low coverage (~30X) with two insert size libraries resulting in an average N50 scaffold size of about 50 kb. Repetitive elements comprised 4%-22% of the bird genomes. The assembled scaffolds allowed the homology-based annotation of 13,000 ~ 17000 protein coding genes in each avian genome relative to chicken, zebra finch and human, as well as comparative and sequence conservation analyses.

Conclusions:

Here we release full genome assemblies of 38 newly sequenced avian species, link genome assembly downloads for the 7 of the remaining 10 species, and provide a guideline of genomic data that has been generated and used in our Avian Phylogenomics Project. To the best of our knowledge, the Avian Phylogenomics Project is the biggest vertebrate comparative genomics project to date. The genomic data presented here is expected to accelerate further analyses in many fields, including phylogenetics, comparative genomics, evolution, neurobiology, development biology, and other related areas.

Viz také:

http://gigadb.org/dataset/101000

http://gigadb.org/dataset/101041

Li C, Zhang Y, Li J, Kong L, Hu H, Pan H, Xu L, Deng Y, Li Q, Jin L, Yu H, Chen Y, Liu B, Yang L, Liu S, Zhang Y, Lang Y, Xia J, He W, Shi Q, Subramanian S, Millar CD, Meader S, Rands CM, Fujita MK, Greenwold MJ, Castoe TA, Pollock DD, Gu W, Nam K, Ellegren H, Ho SYW, Burt DW, Ponting CP, Jarvis ED, Gilbert TMP, Yang H, Wang J, Lambert DM, Wang J, Zhang G 2014 Two Antarctic penguin genomes reveal insights into their evolutionary history and molecular changes related to the cold Antartic environment. GigaScience 3: 27

Background:

Penguins are flightless aquatic birds widely distributed in the Southern Hemisphere. The distinctive morphological and physiological features of penguins allow them to live an aquatic life, and some of them have successfully adapted to the hostile environments in Antarctica. To study the phylogenetic and population history of penguins and the molecular basis of their adaptations to Antarctica, we sequenced the genomes of the two Antarctic dwelling penguin species, the Adélie penguin [Pygoscelis adeliae] and emperor penguin [Aptenodytes forsteri].

Results:

Phylogenetic dating suggests that early penguins arose ~60 million years ago, coinciding with a period of global warming. Analysis of effective population sizes reveals that the two penguin species experienced population expansions from ~1 million years ago to ~100 thousand years ago, but responded differently to the climatic cooling of the last glacial period. Comparative genomic analyses with other available avian genomes identified molecular changes in genes related to epidermal structure, phototransduction, lipid metabolism, and forelimb morphology.

Conclusions:

Our sequencing and initial analyses of the first two penguin genomes provide insights into the timing of penguin origin, fluctuations in effective population sizes of the two penguin species over the past 10 million years, and the potential associations between these biological patterns and global climate change. The molecular changes compared with other avian genomes reflect both shared and diverse adaptations of the two penguin species to the Antarctic environment.

O'Brien SJ, Haussler D, Ryder O 2014 The birds of Genome10K. GigaScience 3: 32

Everyone loves the birds of the world. From their haunting songs and majesty of flight to dazzling plumage and mating rituals, bird watchers - both amateurs and professionals - have marveled for centuries at their considerable adaptations. Now, we are offered a special treat with the publication of a series of papers in dedicated issues of Science, Genome Biology and GigaScience (which also included pre-publication data release). These present the successful beginnings of an international interdisciplinary venture, the Avian Phylogenomics Project that lets us view, through a genomics lens, modern bird species and the evolutionary events that produced them.

BMC Genomics:

Romanov MN, Farré M, Lithgow PE, Fowler KE, Skinner BM, O'Connor R, Fonseka G, Backström N, Matsuda Y, Nishida C, Houde P, Jarvis ED, Ellegren H, Burt DW, Larkin DM, Griffin DK 2014 Reconstruction of gross avian genome structure, organization and evolution suggests that the chicken lineage most closely resembles the dinosaur avian ancestor. BMC Genom 15: 1060

Background:

The availability of multiple avian genome sequence assemblies greatly improves our ability to define overall genome organization and reconstruct evolutionary changes. In birds, this has previously been impeded by a near intractable karyotype and relied almost exclusively on comparative molecular cytogenetics of only the largest chromosomes. Here, novel whole genome sequence information from 21 avian genome sequences (most newly assembled) made available on an interactive browser (Evolution Highway) was analyzed.

Results:

Focusing on the six best-assembled genomes allowed us to assemble a putative karyotype of the dinosaur ancestor for each chromosome. Reconstructing evolutionary events that led to each species' genome organization, we determined that the fastest rate of change occurred in the zebra finch and budgerigar, consistent with rapid speciation events in the Passeriformes and Psittaciformes. Intra- and interchromosomal changes were explained most parsimoniously by a series of inversions and translocations respectively, with breakpoint reuse being commonplace. Analyzing chicken and zebra finch, we found little evidence to support the hypothesis of an association of evolutionary breakpoint regions with recombination hotspots but some evidence to support the hypothesis that microchromosomes largely represent conserved blocks of synteny in the majority of the 21 species analyzed. All but one species showed the expected number of microchromosomal rearrangements predicted by the haploid chromosome count. Ostrich, however, appeared to retain an overall karyotype structure of 2n = 80 despite undergoing a large number (26) of hitherto un-described interchromosomal changes.

Conclusions:

Results suggest that mechanisms exist to preserve a static overall avian karyotype/genomic structure, including the microchromosomes, with widespread interchromosomal change occurring rarely (e.g., in ostrich and budgerigar lineages). Of the species analyzed, the chicken lineage appeared to have undergone the fewest changes compared to the dinosaur ancestor.

Wirthlin M, Lovell PV, Jarvis ED, Mello CV 2014 Comparative genomics reveals molecular features unique to the songbird lineage. BMC Genom 15: 1082

Background 

Songbirds (oscine Passeriformes) are among the most diverse and successful vertebrate groups, comprising almost half of all known bird species. Identifying the genomic innovations that might be associated with this success, as well as with characteristic songbird traits such as vocal learning and the brain circuits that underlie this behavior, has proven difficult, in part due to the small number of avian genomes available until recently. Here we performed a comparative analysis of 48 avian genomes to identify genomic features that are unique to songbirds, as well as an initial assessment of function by investigating their tissue distribution and predicted protein domain structure.

Results

Using BLAT alignments and gene synteny analysis, we curated a large set of Ensembl gene models that were annotated as novel or duplicated in the most commonly studied songbird, the Zebra finch (Taeniopygia guttata), and then extended this analysis to 47 additional avian and 4 non-avian genomes. We identified 10 novel genes uniquely present in songbird genomes. A refined map of chromosomal synteny disruptions in the Zebra finch genome revealed that the majority of these novel genes localized to regions of genomic instability associated with apparent chromosomal breakpoints. Analyses of in situ hybridization and RNA-seq data revealed that a subset of songbird-unique genes is expressed in the brain and/or other tissues, and that 2 of these (YTHDC2L1 and TMRA) are highly differentially expressed in vocal learning-associated nuclei relative to the rest of the brain.

Conclusions 

Our study reveals novel genes unique to songbirds, including some that may subserve their unique vocal control system, substantially improves the quality of Zebra finch genome annotations, and contributes to a better understanding of how genomic features may have evolved in conjunction with the emergence of the songbird lineage.

BMC Evolutionary Biology:

Greenwold MJ, Bao W, Jarvis ED, Hu H, Li C, Gilbert MTP, Zhang G, Sawyer RH 2014 Dynamic evolution of the alpha (α) and beta (β) keratins has accompanied integument diversification and the adaptation of birds into novel lifestyles. BMC Evol Biol 14: 249

Background:

Vertebrate skin appendages are constructed of keratins produced by multigene families. Alpha (α) keratins are found in all vertebrates, while beta (β) keratins are found exclusively in reptiles and birds. We have studied the molecular evolution of these gene families in the genomes of 48 phylogenetically diverse birds and their expression in the scales and feathers of the chicken.

Results:

We found that the total number of α-keratins is lower in birds than mammals and non-avian reptiles, yet two α-keratin genes (KRT42 and KRT75) have expanded in birds. The β-keratins, however, demonstrate a dynamic evolution associated with avian lifestyle. The avian specific feather β-keratins comprise a large majority of the total number of β-keratins, but independently derived lineages of aquatic and predatory birds have smaller proportions of feather β-keratin genes and larger proportions of keratinocyte β-keratin genes. Additionally, birds of prey have a larger proportion of claw β-keratins. Analysis of α- and β-keratin expression during development of chicken scales and feathers demonstrates that while α-keratins are expressed in these tissues, the number and magnitude of expressed β-keratin genes far exceeds that of α-keratins.

Conclusions:

These results support the view that the number of α- and β-keratin genes expressed, the proportion of the β-keratin subfamily genes expressed and the diversification of the β-keratin genes have been important for the evolution of the feather and the adaptation of birds into multiple ecological niches.

Wang Z, Zhang J, Yang W, An N, Zhang P, Zhang G, Zhou Q 2014 Temporal genomic evolution of bird sex chromosomes. BMC Evol Biol 14: 250

Background:

Sex chromosomes exhibit many unusual patterns in sequence and gene expression relative to autosomes. Birds have evolved a female heterogametic sex system (male ZZ, female ZW), through stepwise suppression of recombination between chrZ and chrW. To address the broad patterns and complex driving forces of Z chromosome evolution, we analyze here 45 newly available bird genomes and four species’ transcriptomes, over their course of recombination loss between the sex chromosomes.

Results:

We show Z chromosomes in general have a significantly higher substitution rate in introns and synonymous protein-coding sites than autosomes, driven by the male-to-female mutation bias (‘male-driven evolution’ effect). Our genome-wide estimate reveals that the degree of such a bias ranges from 1.6 to 3.8 among different species. G + C content of third codon positions exhibits the same trend of gradual changes with that of introns, between chrZ and autosomes or regions with increasing ages of becoming Z-linked, therefore codon usage bias in birds is probably driven by the mutational bias. On the other hand, Z chromosomes also evolve significantly faster at nonsynonymous sites relative to autosomes (‘fast-Z’ evolution). And species with a lower level of intronic heterozygosities tend to evolve even faster on the Z chromosome. Further analysis of fast-evolving genes’ enriched functional categories and sex-biased expression patterns support that, fast-Z evolution in birds is mainly driven by genetic drift. Finally, we show in species except for chicken, gene expression becomes more male-biased within Z-linked regions that have became hemizygous in females for a longer time, suggesting a lack of global dosage compensation in birds, and the reported regional dosage compensation in chicken has only evolved very recently.

Conclusions:

In conclusion, we uncover that the sequence and expression patterns of Z chromosome genes covary with their ages of becoming Z-linked. In contrast to the mammalian X chromosomes, such patterns are mainly driven by mutational bias and genetic drift in birds, due to the opposite sex-biased inheritance of Z vs. X.

PLOS ONE:

Pereira J, Johnson WE, O’Brien SJ, Jarvis ED, Zhang G, Gilbert MTP, Vasconcelos V, Antunes A 2014 Evolutionary genomics and adaptive evolution of the hedgehog gene family (Shh, Ihh, and Dhh) in vertebrates. PLOS ONE 9(12): e74132

The Hedgehog (Hh) gene family codes for a class of secreted proteins composed of two active domains that act as signalling molecules during embryo development, namely for the development of the nervous and skeletal systems and the formation of the testis cord. While only one Hh gene is found typically in invertebrate genomes, most vertebrates species have three (Sonic hedgehog – Shh; Indian hedgehog – Ihh; and Desert hedgehog – Dhh), each with different expression patterns and functions, which likely helped promote the increasing complexity of vertebrates and their successful diversification. In this study, we used comparative genomic and adaptive evolutionary analyses to characterize the evolution of the Hh genes in vertebrates following the two major whole genome duplication (WGD) events. To overcome the lack of Hh-coding sequences on avian publicly available databases, we used an extensive dataset of 45 avian and three non-avian reptilian genomes to show that birds have all three Hh paralogs. We find suggestions that following the WGD events, vertebrate Hh paralogous genes evolved independently within similar linkage groups and under different evolutionary rates, especially within the catalytic domain. The structural regions around the ion-binding site were identified to be under positive selection in the signaling domain. These findings contrast with those observed in invertebrates, where different lineages that experienced gene duplication retained similar selective constraints in the Hh orthologs. Our results provide new insights on the evolutionary history of the Hh gene family, the functional roles of these paralogs in vertebrate species, and on the location of mutational hotspots.

Genome Biology and Evolution:

Suh A, Churakov G, Ramakodi MP, Platt II RN, Jurka J, Kojima KK, Caballero J, Smit AF, Vliet KA, Hoffmann FG, Brosius J, Green RE, Braun EL, Ray DA, Schmitz J 2014 Multiple lineages of ancient CR1 retroposons shaped the early genome evolution of amniotes. Genome Biol Evol 7(1): 205–17

Chicken repeat 1 (CR1) retroposons are Long INterspersed Elements (LINEs) that are ubiquitous within amniote genomes and constitute the most abundant family of transposed elements in birds, crocodilians, turtles, and snakes. They are also present in mammalian genomes, where they reside as numerous relics of ancient retroposition events. Yet, despite their relevance for understanding amniote genome evolution, the diversity and evolution of CR1 elements has never been studied on an amniote-wide level. We reconstruct the temporal and quantitative activity of CR1 subfamilies via presence/absence analyses across crocodilian phylogeny and comparative analyses of twelve crocodilian genomes, revealing relative genomic stasis of retroposition during genome evolution of extant Crocodylia. Our large-scale phylogenetic analysis of amniote CR1 subfamilies suggest the presence of at least seven ancient CR1 lineages in the amniote ancestor; and amniote-wide analyses of CR1 successions and quantities reveal differential retention (presence of ancient relics or recent activity) of these CR1 lineages across amniote genome evolution. Interestingly, birds and lepidosaurs retained the fewest ancient CR1 lineages among amniotes and also exhibit smaller genome sizes. Our study is the first to analyze CR1 evolution in a genome-wide and amniote-wide context and the data strongly suggest that the ancestral amniote genome contained myriad CR1 elements from multiple ancient lineages, and remnants of these are still detectable in the relatively stable genomes of crocodilians and turtles. Early mammalian genome evolution was thus characterized by a drastic shift from CR1 prevalence to dominance and hyperactivity of L2 LINEs in monotremes and L1 LINEs in therians.

Journal of Comparative Neurology:

Wang R, Chen C-C, Hara E, Rivas MV, Roulhac PL, Howard JT, Chakraborty M, Audet J-N, Jarvis ED 2014 Convergent differential regulation of SLIT-ROBO axon guidance genes in the brains of vocal learners. 523(6): 892–906

Only a few distantly related mammals and birds have the trait of complex vocal learning, which is the ability to imitate novel sounds. This ability is critical for speech acquisition and production in humans, and is attributed to specialized forebrain vocal control circuits that have several unique connections relative to adjacent brain circuits. As a result, it has been hypothesized that there could exist convergent changes in genes involved in neural connectivity of vocal learning circuits. In support of this hypothesis, expanding on our related study (Pfenning et al. [2014] Science 346: 1256846), here we show that the forebrain part of this circuit that makes a relatively rare direct connection to brainstem vocal motor neurons in independent lineages of vocal learning birds (songbird, parrot, and hummingbird) has specialized regulation of axon guidance genes from the SLIT-ROBO molecular pathway. The SLIT1 ligand was differentially downregulated in the motor song output nucleus that makes the direct projection, whereas its receptor ROBO1 was developmentally upregulated during critical periods for vocal learning. Vocal non-learning bird species and male mice, which have much more limited vocal plasticity and associated circuits, did not show comparable specialized regulation of SLIT-ROBO genes in their non-vocal motor cortical regions. These findings are consistent with SLIT and ROBO gene dysfunctions associated with autism, dyslexia, and speech sound language disorders and suggest that convergent evolution of vocal learning was associated with convergent changes in the SLIT-ROBO axon guidance pathway.

Zdroje:

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