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Persoonia : Molecular Phylogeny and Evolution of Fungi logoLink to Persoonia : Molecular Phylogeny and Evolution of Fungi
. 2009 Jun 5;22:129–138. doi: 10.3767/003158509X461486

Geoglossomycetes cl. nov., Geoglossales ord. nov. and taxa above class rank in the Ascomycota Tree of Life

CL Schoch 1,✉, Z Wang 2, JP Townsend 2, JW Spatafora 3
PMCID: PMC2776753  NIHMSID: NIHMS133499  PMID: 19915689

Abstract

Featuring a high level of taxon sampling across Ascomycota, we evaluate a multi-gene phylogeny and propose a novel order and class in Ascomycota. We describe two new taxa, Geoglossomycetes and Geoglossales, to host three earth tongue genera: Geoglossum, Trichoglossum and Sarcoleotia as a lineage of ‘Leotiomyceta’. Correspondingly, we confirm that these genera are not closely related to the genera Neolecta, Mitrula, Cudonia, Microglossum, Thuemenidum, Spathularia and Bryoglossum, all of which have been previously placed within the Geoglossaceae. We also propose a non-hierarchical system for naming well-resolved nodes, such as ‘Saccharomyceta’, ‘Dothideomyceta’, and ‘Sordariomyceta’ for supraordinal nodes, within the current phylogeny, acting as rankless taxa. As part of this revision, the continued use of ‘Leotiomyceta’, now as a rankless taxon, is proposed.

Keywords: Bayesian inference, hybrid classification, maximum likelihood

INTRODUCTION

The multi-gene sequence datasets generated by the research consortium ‘Assembling the Fungal Tree of Life’ (AFTOL) have resulted in several multi-gene phylogenies incorporating comprehensive taxon sampling across Fungi (Lutzoni et al. 2004, Blackwell et al. 2006, James et al. 2006). AFTOL generated a data matrix spanning all currently accepted classes in the Ascomycota, the largest fungal phylum. The phylogenies produced by AFTOL prompted the proposal of a phylogenetic classification from phylum to ordinal level in fungi (Hibbett et al. 2007). Although the Botanical Code does not require the principle of priority in ranks above family (McNeill et al. 2006), this principle was nevertheless followed for all taxa. The following ranked taxa were defined: subkingdom, phylum (suffix -mycota, except for Microsporidia), subphylum (-mycotina), class (-mycetes), subclass (-mycetidae) and order (-ales). As in Hibbett et al. (2007), several phylogenetically well-supported nodes above the rank of order could not be accommodated in the current hierarchical classification system based on the International Code of Botanical Nomenclature. To remedy this deficiency, rankless (or unranked) taxa for unambiguously resolved nodes with strong statistical support was proposed (Hibbett & Donoghue 1998). Hybrid classifications that include both rankless and Linnaean taxa have since been discussed elsewhere (Jørgensen 2002, Kuntner & Agnarsson 2006), and applied to diverse organisms from lichens (Stenroos et al. 2002) and plants (Sennblad & Bremer 2002, Pfeil & Crisp 2005) to spiders (Kuntner 2006). These studies all attempt to create a comprehensive code for phylogenetic nomenclature that retains the current Linnean hierarchical codes.

In keeping with the practice of previous hybrid classifications, we propose to use names corresponding to clades of higher taxa that were resolved in this phylogeny as well as preceding studies. The proposed informal, rankless names for well-supported clades above the class level in our phylogeny agrees with the principles of the Phylocode (http://www.ohio.edu/phylocode/). It is our hope that such names should function as rankless taxa, facilitating the naming of additional nodes/clades as they become resolved. Eventual codification will follow the example of Hibbett et al. (2007) by applying principles of type names and priority. A number of published manuscripts already provide background on other supraordinal relationships of Fungi; for more complete treatments of the various classes, see Blackwell et al. (2006).

During the AFTOL project a data matrix was generated spanning all currently accepted classes in the Ascomycota, the largest fungal phylum. A multi-gene phylogeny was recently inferred from these data, demonstrating relevant patterns in biological and morphological character development as well as establishing several distinct lineages in Ascomycota (Schoch et al. 2009). Here we test whether the relationships reported in Schoch et al. (2009) remain valid by applying both maximum likelihood (ML) and Bayesian analyses on a more restricted but denser set of taxa, including expanded sampling in the Geoglossaceae.

We will therefore address the taxonomic placement of a group of fungi with earth tongue morphologies that are shown to be unrelated to other known classes. This morphology is closely associated with the family Geoglossaceae (Corda 1838). With typical inoperculate asci and an exposed hymenium, Geoglossaceae has long been thought to be a member of Leotiomycetes, though the content of the family itself has experienced many changes (Nannfeldt 1942, Korf 1973, Spooner 1987, Platt 2000, Wang et al. 2006a, b). It is currently listed with 48 species and 6 genera in the Dictionary of the Fungi (Kirk et al. 2008). Several analyses using molecular data supported a clade including three earth tongue genera, Geoglossum, Trichoglossum and Sarcoleotia (Fig. 1), and cast doubt upon their positions in Leotiomycetes (Platt 2000, Gernandt et al. 2001, Lutzoni et al. 2004, Sandnes 2006, Spatafora et al. 2006, Wang et al. 2006b). Here we present a comprehensive phylum-wide phylogeny, including data from protein coding genes. We can confidently place the earth tongue family as separate from currently accepted classes in Ascomycota.

Fig. 1.

Fig. 1

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A most likely tree obtained by RAxML for Ascomycota. Subphyla, class and rankless taxa are indicated. Classes containing fungi designated as earth tongues are indicated in black. The tree was rooted with outgroup Rhizopus oryzae (not shown). Bootstrap values are shown in orange and Bayesian posterior probabilities in blue. Orange, bold branches are supported by more than 80 % bootstrap and 95 % posterior probability, respectively. The full phylogeny, without collapsed clades, are shown in Fig. 2. The inset figures illustrate morphological ascomal diversity in the earth tongues. The species are as follows: A. Trichoglossum hirsutum; B. Geoglossum nigritum; C. Microglossum rufum; D. Spathularia velutipes; E. Geoglossum nigritum. Photo credits: A: Zhuliang Yang; B, D, E: Kentaro Hosaka; C: Dan Luoma.

MATERIALS AND METHODS

Data were extracted from the complete data matrix obtained from the WASABI database (www.aftol.org), incorporating representatives for all currently accepted classes, and maximizing the number of orders and available data. Following the approach of James et al. (2006) we performed a combined analysis, with both DNA and amino acid data, while allowing for missing data. This data was supplemented with additional ribosomal sequences from earth tongue genera obtained and deposited in GenBank from two previous studies (Wang et al. 2006a, b). To further minimise poorly aligned areas, 219 additional columns, which proved variable when viewed in BioEdit with a 40 % shade threshold, were excluded from the original AFTOL inclusion set. The refined dataset consisted of 161 taxa (including outgroups) and 4 429 characters for six different loci: the nuclear small and large ribosomal subunits (nSSU, nLSU), the mitochondrial small ribosomal subunit (mSSU) and fragments from three proteins: transcription elongation factor 1 alpha (TEF1) and the largest and second largest subunits of RNA polymerase II (RPB1, RPB2). A complete table with the published GenBank numbers is listed in Table 1.

Table 1.

Taxa and sequences used in this study.

AFTOL no. Class Order Voucher1 Taxon nSSU nLSU mSSU RPB1 RPB2 TEF1
1241 Zygomycota outgroup GB Rhizopus oryzae AF113440 AY213626 AY863212 Genome Genome Genome
438 Basidiomycota outgroup GEL 5359 Calocera cornea AY771610 AY701526 AY857980 AY536286 AY881019
439 Basidiomycota outgroup AW 136 Calostoma cinnabarinum AY665773 AY645054 AY857979 AY780939 AY879117
1088 Basidiomycota outgroup GB Cryptococcus neoformans Genome Genome XM_570943 XM_570204 Genome
770 Basidiomycota outgroup MB 03-036 Fomitopsis pinicola AY705967 AY684164 FJ436112 AY864874 AY786056 AY885152
701 Basidiomycota outgroup DSH s.n. Grifola frondosa AY705960 AY629318 AY864876 AY786057 AY885153
126 Arthoniomycetes Arthoniales Diederich 15572 Roccella fuciformis AY584678 AY584654 EU704082 DQ782825 DQ782866
93 Arthoniomycetes Arthoniales BG Printzen1981 Roccellographa cretacea DQ883705 DQ883696 FJ772240 DQ883713 DQ883733
307 Arthoniomycetes Arthoniales DUKE 0047570 Schismatomma decolorans AY548809 AY548815 AY548816 DQ883718 DQ883715 DQ883725
946 Dothideomycetes Botryosphaeriales CBS 115476 Botryosphaeria dothidea DQ677998 DQ678051 FJ190612 EU186063 DQ677944 DQ767637
1586 Dothideomycetes Botryosphaeriales CBS 418.64 Botryosphaeria tsugae AF271127 DQ767655 DQ767644 DQ677914
1618 Dothideomycetes Botryosphaeriales CBS 237.48 Guignardia bidwellii DQ678034 DQ678085 DQ677983
1784 Dothideomycetes Botryosphaeriales CBS 447.70 Guignardia gaultheriae DQ678089 FJ190646 DQ677987
939 Dothideomycetes Capnodiales CBS 147.52 Capnodium coffeae DQ247808 DQ247800 FJ190609 DQ471162 DQ247788 DQ471089
1289 Dothideomycetes Capnodiales CBS 170.54 Cladosporium cladosporioides DQ678004 DQ678057 FJ190628 EU186064 DQ677952 DQ677898
1591 Dothideomycetes Capnodiales CBS 399.80 Davidiella tassiana DQ678022 DQ678074 DQ677971 DQ677918
2021 Dothideomycetes Capnodiales OSC 100622 Mycosphaerella fijiensis DQ767652 DQ678098 FJ190656 DQ677993
1615 Dothideomycetes Capnodiales CBS 292.38 Mycosphaerella graminicola DQ678033 DQ678084 DQ677982
942 Dothideomycetes Capnodiales CBS 113265 Mycosphaerella punctiformis DQ471017 DQ470968 FJ190611 DQ471165 DQ470920 DQ471092
1594 Dothideomycetes Capnodiales CBS 325.33 Scorias spongiosa DQ678024 DQ678075 FJ190643 DQ677973 DQ677920
274 Dothideomycetes Dothideales DAOM 231303 Dothidea sambuci AY544722 AY544681 AY544739 DQ522854 DQ497606
1359 Dothideomycetes Dothideales CBS 737.71 Dothiora cannabinae DQ479933 DQ470984 FJ190636 DQ471182 DQ470936 DQ471107
1300 Dothideomycetes Dothideales CBS 116.29 Sydowia polyspora DQ678005 DQ678058 FJ190631 DQ677953 DQ677899
Dothideomycetes Hysteriales CBS 114601 Gloniopsis smilacis FJ161135 FJ161174 FJ161114 FJ161091
Dothideomycetes Hysteriales EB 0324 Hysterium angustatum FJ161167 FJ161207 FJ161129 FJ161111
Dothideomycetes Hysteriales EB 0249 Hysterographium mori FJ161155 FJ161196 FJ161104
1613 Dothideomycetes Incertae sedis CBS 283.51 Helicomyces roseus DQ678032 DQ678083 DQ677981 DQ677928
1580 Dothideomycetes Incertae sedis CBS 245.49 Tubeufia paludosa DQ767649 DQ767654 DQ767643 DQ767638
1853 Dothideomycetes Myriangiales CBS 150.27 Elsinoë veneta DQ767651 DQ767658 FJ190650 DQ767641
1304 Dothideomycetes Myriangiales CBS 260.36 Myriangium duriaei AY016347 DQ678059 AY571389 DQ677954 DQ677900
Dothideomycetes Mytilinidiales EB 0248 Lophium mytilinum FJ161163 FJ161203 FJ161128 FJ161110
Dothideomycetes Mytilinidiales CBS 301.34 Mytilinidion australe FJ161183
Dothideomycetes Mytilinidiales CBS 135.34 Mytilinidion rhenanum FJ161136 FJ161175 FJ161115 FJ161092
267 Dothideomycetes Pleosporales DAOM 195275 Allewia eureka DQ677994 DQ678044 DQ677938 DQ677883
1583 Dothideomycetes Pleosporales CBS 126.54 Ascochyta pisi var. pisi DQ678018 DQ678070 DQ677967 DQ677913
54 Dothideomycetes Pleosporales CBS 134.39 Cochliobolus heterostrophus AY544727 AY544645 AY544737 DQ247790 DQ497603
1599 Dothideomycetes Pleosporales CBS 225.62 Delitschia winteri DQ678026 DQ678077 FJ190644 DQ677975 DQ677922
1576 Dothideomycetes Pleosporales CBS 101341 Lepidosphaeria nicotiae DQ678067 DQ677963 DQ677910
277 Dothideomycetes Pleosporales DAOM 229267 Leptosphaeria maculans DQ470993 DQ470946 DQ471136 DQ470894 DQ471062
1575 Dothideomycetes Pleosporales CBS 276.37 Phoma herbarum DQ678014 DQ678066 FJ190640 DQ677962 DQ677909
1600 Dothideomycetes Pleosporales CBS 279.74 Pleomassaria siparia DQ678027 DQ678078 DQ677976 DQ677923
940 Dothideomycetes Pleosporales CBS 541.72 Pleospora herbarum var. herbarum DQ247812 DQ247804 FJ190610 DQ471163 DQ247794 DQ471090
283 Dothideomycetes Pleosporales DAOM 222769 Pyrenophora phaeocomes DQ499595 DQ499596 FJ190591 DQ497614 DQ497607
1256 Dothideomycetes Pleosporales CBS 524.50 Sporormiella minima DQ678003 DQ678056 FJ190624 DQ677950 DQ677897
1598 Dothideomycetes Pleosporales CBS 110020 Ulospora bilgramii DQ678025 DQ678076 DQ677974 DQ677921
1601 Dothideomycetes Pleosporales CBS 304.66 Verruculina enalia DQ678028 DQ678079 DQ677977 DQ677924
1037 Dothideomycetes Pleosporales CBS 454.72 Westerdykella cylindrica AY016355 AY004343 AF346430 DQ471168 DQ470925 DQ497610
1063 Eurotiomycetes Chaetothyriales CBS 175.95 Ceramothyrium carniolicum EF413627 EF413628 EF413629 EF413630
1033 Eurotiomycetes Chaetothyriales CBS190.61 Cyphellophora laciniata EF413618 EF413619
671 Eurotiomycetes Chaetothyriales CBS 157.67 Exophiala salmonis EF413608 EF413609 FJ225745 EF413610 EF413611 EF413612
1911 Eurotiomycetes Coryneliales CBS 138.64 Caliciopsis orientalis DQ471039 DQ470987 FJ190654 DQ471185 DQ470939 DQ471111
5007 Eurotiomycetes Eurotiales CBS 658.74 Aspergillus protuberus FJ176842 FJ176897 FJ238379
2014 Eurotiomycetes Eurotiales CBS 339.97 Eupenicillium limosum EF411061 EF411064 EF411068 EF411070
1083 Eurotiomycetes Onygenales GB Ajellomyces capsulatum Genome Genome Genome Genome Genome
1084 Eurotiomycetes Onygenales TIGR Coccidioides immitis Genome Genome Genome Genome Genome
684 Eurotiomycetes Verrucariales NYBG 808041 Agonimia sp. DQ782885 DQ782913 DQ782853 DQ782874 DQ782917
697 Eurotiomycetes Verrucariales DUKE 0047959 Staurothele frustulenta DQ823105 DQ823098 FJ225702 DQ840553 DQ840560
Geoglossomycetes Geoglossales OSC 60610 Geoglossum glabrum AY789316 AY789317
56 Geoglossomycetes Geoglossales OSC 100009 Geoglossum nigritum AY544694 AY544650 AY544740 DQ471115 DQ470879 DQ471044
Geoglossomycetes Geoglossales Mycorec1840 Geoglossum umbratile AY789302 AY789321
Geoglossomycetes Geoglossales HMAS 71956 Sarcoleotia globosa 1 AY789298 AY789299
Geoglossomycetes Geoglossales OSC 63633 Sarcoleotia globosa 2 AY789409
Geoglossomycetes Geoglossales MBH 52476 Sarcoleotia globosa 3 AY789428
64 Geoglossomycetes Geoglossales OSC 100017 Trichoglossum hirsutum 1 AY544697 AY544653 AY544758 DQ471119 DQ470881 DQ471049
Geoglossomycetes Geoglossales OSC 61726 Trichoglossum hirsutum 2 AY789312 AY789313
229 Incertae sedis Incertae sedis IAM 12963 Saitoella complicata AY548297 AY548296 DQ471133 AY548300 DQ471133
Laboulbeniomycetes Laboulbeniales GB Hesperomyces virescens AF298233 AF298235
Laboulbeniomycetes Laboulbeniales GB Stigmatomyces protrudens AF298232 AF298234
2197 Laboulbeniomycetes Pyxidiophorales CBS 657.82 Pyxidiophora avernensis FJ176839 FJ176894 FJ238377 FJ238412
962 Lecanoromycetes Agyriales GB Trapelia placodioides AF119500 AF274103 AF431962 DQ366259 DQ366260 DQ366258
589 Lecanoromycetes Incertae sedis DUKE 0047522 Lecidea fuscoatra DQ912310 DQ912332 DQ912275 DQ912355 DQ912381
6 Lecanoromycetes Lecanorales DUKE 0047740 Canoparmelia caroliniana AY584658 AY584634 AY584613 DQ782817 AY584683 DQ782889
195 Lecanoromycetes Lecanorales DUKE 0047550 Hypogymnia physodes DQ973006 DQ973030 DQ972978 DQ973091
958 Lecanoromycetes Ostropales s.l. Lumbsch 995 Diploschistes ocellatus AF038877 AY605077 DQ366252 DQ366253 DQ366251
1349 Lecanoromycetes Ostropales s.l. JK 5548K Glomerobolus gelineus DQ247811 DQ247803 DQ247784 DQ247793
128 Lecanoromycetes Peltigerales DUKE 0047503 Lobaria scrobiculata AY584679 AY584655 AY584621 DQ883736 DQ883749 DQ883768
314 Lecanoromycetes Peltigerales DUKE 0047520 Lobariella pallida DQ883788 DQ883797 DQ912297 DQ883740 DQ883753 DQ883772
131 Lecanoromycetes Peltigerales DUKE 0047548 Nephroma parile 46411421 46411445 46411390 DQ973061 DQ973075 FJ772246
134 Lecanoromycetes Peltigerales DUKE 0047504 Peltigera degenii AY584681 AY584657 AY584628 DQ782826 AY584688 DQ782897
333 Lecanoromycetes Peltigerales DUKE 0047747 Coccocarpia erythroxyli DQ883791 DQ883800 DQ912294 DQ883743 DQ883756 DQ883775
875 Lecanoromycetes Pertusariales DUKE 0047641 Icmadophila ericetorum DQ883704 DQ883694 DQ986897 DQ883723 DQ883711 DQ883730
224 Lecanoromycetes Pertusariales DUKE 0047506 Pertusaria dactylina DQ782880 DQ782907 DQ972973 DQ782828 DQ782868 DQ782899
320 Lecanoromycetes Teloschistales DUKE 0047507 Heterodermia vulgaris DQ883789 DQ883798 DQ912288 DQ883741 DQ883754 DQ883773
686 Lecanoromycetes Teloschistales DUKE 0047544 Pyxine subcinerea DQ883793 DQ883802 DQ912292 DQ883745 DQ883758 DQ883777
87 Lecanoromycetes Teloschistales DUKE 0047925 Teloschistes exilis AY584671 AY584647 FJ772245 DQ883779 DQ883759 DQ883764
59 Leotiomycetes Helotiales OSC 100012 Botryotinia fuckeliana AY544695 AY544651 AY544732 DQ471116 DQ247786 DQ471045
Leotiomycetes Helotiales MBH 52481 Bryoglossum gracile AY789419 AY789420
166 Leotiomycetes Helotiales OSC 100054 Cudoniella cf. clavus DQ470992 DQ470944 FJ713604 DQ471128 DQ470888 DQ471056
941 Leotiomycetes Helotiales CBS 161.38 Dermea acerina DQ247809 DQ247801 DQ976373 DQ471164 DQ247791 DQ471091
49 Leotiomycetes Helotiales OSC 100002 Lachnum virgineum AY544688 AY544646 AY544745 DQ842030 DQ470877 DQ497602
1262 Leotiomycetes Helotiales CBS 811.85 Lambertella subrenispora DQ471030 DQ470978 DQ471176 DQ470930 DQ471101
1 Leotiomycetes Helotiales OSC 100001 Leotia lubrica AY544687 AY544644 AY544746 DQ471113 DQ470876 DQ471041
Leotiomycetes Helotiales FH-DSH -97103 Microglossum olivaceum AY789396 AY789397
Leotiomycetes Helotiales Ingo-Clark-Geo163 Microglossum rufum 1 DQ257358 DQ257359
1292 Leotiomycetes Helotiales OSC 100641 Microglossum rufum 2 DQ471033 DQ470981 DQ471179 DQ470933 DQ471104
Leotiomycetes Helotiales ZW02-012 Mitrula brevispora AY789292 AY789293
Leotiomycetes Helotiales WZ-Geo47-Clark Mitrula elegans AY789334 AY789335
169 Leotiomycetes Helotiales OSC 100063 Monilinia laxa AY544714 AY544670 AY544748 FJ238425 DQ470889 DQ471057
1259 Leotiomycetes Helotiales CBS 477.97 Neobulgaria pura FJ176865 FJ238434 FJ238350 FJ238397
149 Leotiomycetes Helotiales OSC 100036 Neofabraea malicorticis AY544706 AY544662 AY544751 DQ471124 DQ470885 DQ847414
Leotiomycetes Helotiales 1100803 Thueminidium atropurpureum 1 AY789307
Leotiomycetes Helotiales 1136126 Thueminidium atropurpureum 2 AY789305
353 Leotiomycetes Rhytismatales DUKE 0047585 Cudonia circinans AF107343 AY533013 AY584700 AY641033
Leotiomycetes Rhytismatales OSC 100640 Spathularia velutipes 1 FJ997860 FJ997861 FJ997863 FJ997862
Leotiomycetes Rhytismatales ZW Geo58 Spathularia velutipes 2 AY789356 AY789357
896 Lichinomycetes Lichinales Schultz16319a Lichinella iodopulchra DQ782857 DQ832328 DQ832327
892 Lichinomycetes Lichinales DUKE 0047648 Peltula auriculata DQ832332 DQ832330 DQ782856 DQ832331
891 Lichinomycetes Lichinales DUKE 0047527 Peltula umbilicata DQ782887 DQ832334 DQ922954 DQ782855 DQ832335 DQ782919
1363 Neolectomycetes Neolectales DAH-3 Neolecta irregularis DQ842040 DQ470986 DQ471109
1362 Neolectomycetes Neolectales DAH-11 Neolecta vitellina DQ471037 DQ470985 AAF19058
1252 Orbiliomycetes Orbiliales CBS 397.93 Arthrobotrys elegans FJ176810 FJ176864 FJ238349 FJ238395
905 Orbiliomycetes Orbiliales CBS 917.72 Orbilia vinosa DQ471000 DQ470952 DQ471145 DQ471071
65 Pezizomycetes Pezizales OSC 100018 Aleuria aurantia AY544698 AY544654 DQ471120 DQ247785 DQ466085
70 Pezizomycetes Pezizales KH-00-08 Ascobolus carbonarius AY544720 AY544677 FJ238423
152 Pezizomycetes Pezizales OSC 100062 Caloscypha fulgens DQ247807 DQ247799 DQ471126 DQ247787 DQ471054
933 Pezizomycetes Pezizales CBS 626.71 Eleutherascus lectardii DQ471014 DQ470966 FJ190606 DQ471160 DQ470918 DQ471088
176 Pezizomycetes Pezizales OSC 100068 Gyromitra californica AY544717 AY544673 AY544741 DQ471130 DQ470891 DQ471059
507 Pezizomycetes Pezizales TL-6398 Peziza vesiculosa DQ470995 DQ470948 DQ471140 DQ470898 DQ471066
949 Pezizomycetes Pezizales CBS 666.88 Pyronema domesticum DQ247813 DQ247805 FJ190613 DQ471166 DQ247795 DQ471093
1299 Pezizomycetes Pezizales CBS 472.80 Saccobolus dilutellus FJ176814 FJ176870 FJ238436 FJ238353 FJ238402
954 Pezizomycetes Pezizales CBS 733.68 Sarcosoma latahense FJ176806 FJ176860 FJ238424 FJ238392
153 Pezizomycetes Pezizales OSC 100049 Sarcosphaera crassa AY544712 AY544668 FJ238430
62 Pezizomycetes Pezizales OSC 100015 Scutellinia scutellata DQ247814 DQ247806 FJ190587 DQ479935 DQ247796 DQ471047
74 Pezizomycetes Pezizales NRRL 22338 Verpa conica AY544710 AY544666 AY544761 FJ238389
1073 Saccharomycetes Saccharomycetales GB Candida glabrata AY198398 AY198398 XM_447415 XM_448959 Genome
1269 Saccharomycetes Saccharomycetales GB Candida tropicalis M55527 Genome Genome Genome Genome
1077 Saccharomycetes Saccharomycetales GB Debaryomyces hansenii DHA508273 AF485980 XM_456921 CR382139 Genome
1072 Saccharomycetes Saccharomycetales GB Eremothecium gossypii AE016820 AE016820 AF442353 NM_209535 AE016819 Genome
1069 Saccharomycetes Saccharomycetales GB Saccharomyces cerevisiae SCYLR154C SCYLR154C AF442281 X96876 SCYOR151C Genome
1199 Schizosaccharomycetes Schizosaccharomycetales GB Schizosaccharomyces pombe X54866 Z19136 X54421 X56564 D13337 Genome
5086 Sordariomycetes Calosphaeriales CBS 115999 Calosphaeria pulchella AY761071 AY761075 FJ238421
Sordariomycetes Coronophorales SMH4320 Bertia moriformis AY695260 AY780151
2124 Sordariomycetes Diaporthales CBS 171.69 Cryptosporella hypodermia DQ862049 DQ862028 DQ862018 DQ862034
935 Sordariomycetes Diaporthales CBS 109767 Diaporthe eres DQ471015 AF408350 FJ190607 DQ471161 DQ470919 DQ479931
1223 Sordariomycetes Diaporthales CBS 112915 Endothia gyrosa DQ471023 DQ470972 DQ471169 DQ470926 DQ471096
952 Sordariomycetes Diaporthales CBS 199.53 Gnomonia gnomon DQ471019 AF408361 FJ190615 DQ471167 DQ470922 DQ471094
187 Sordariomycetes Hypocreales GJS 71-328 Bionectria cf. aureofulva DQ862044 DQ862027 FJ713625 DQ862013 DQ862029
189 Sordariomycetes Hypocreales GAM 12885 Claviceps purpurea AF543765 AF543789 AY489648 DQ522417 AF543778
162 Sordariomycetes Hypocreales OSC 93609 Cordyceps cardinalis AY184973 AY184962 EF469007 DQ522370 DQ522422 DQ522325
192 Sordariomycetes Hypocreales OSC 71233 Elaphocordyceps capitata AY489689 AY489721 FJ713628 AY489649 DQ522421 AY489615
193 Sordariomycetes Hypocreales OSC 106405 Elaphocordyceps ophioglossoides AY489691 AY489723 FJ713629 AY489652 DQ522429 AY489618
163 Sordariomycetes Hypocreales ATCC 56429 Epichloë typhina U32405 U17396 FJ713624 DQ522440 AF543777
156 Sordariomycetes Hypocreales ATCC 208838 Hypocrea lutea AF543768 AF543791 FJ713620 AY489662 DQ522446 AF543781
159 Sordariomycetes Hypocreales CBS 114055 Nectria cinnabarina U32412 U00748 FJ713622 AY489666 DQ522456 AF543785
1265 Sordariomycetes Incertae sedis FAU 553 Glomerella cingulata AF543762 AF543786 FJ190626 AY489659 DQ522441 AF543773
237 Sordariomycetes Incertae sedis ATCC 16535 Verticillium dahliae AY489705 DQ470945 FJ713630 AY489673 DQ522468 AY489632
413 Sordariomycetes Lulworthiales JK 5090A Lindra thalassiae DQ470994 DQ470947 FJ190593 DQ471139 DQ470897 DQ471065
747 Sordariomycetes Lulworthiales JK 4686 Lulworthia grandispora DQ522855 DQ522856 FJ190595 DQ518181 DQ497608
734 Sordariomycetes Magnaporthales JK 5528S Gaeumannomyces medullaris FJ176801 FJ176854
1081 Sordariomycetes Magnaporthales Broad Magnaporthe grisea AB026819 AB026819 Genome Genome Genome
Sordariomycetes Melanosporales ATCC 15515 Melanospora tiffanyae AY015619 AY015630 AY015637
1906 Sordariomycetes Microascales TCH C89 Ceratocystis fimbriata U32418 U17401 FJ238372
5011 Sordariomycetes Microascales 728a Corollospora maritima FJ176846 FJ176901 FJ190660 FJ238381 FJ238415
1907 Sordariomycetes Microascales CBS 122611 Gondwanamyces capensis FJ176834 FJ176888 FJ238373
409 Sordariomycetes Microascales CBS 197.60 Halosphaeria appendiculata U46872 U46885 FJ238390
1038 Sordariomycetes Ophiostomatales CBS 139.51 Ophiostoma stenoceras DQ836897 DQ836904 FJ190618 DQ836891 DQ836912
1078 Sordariomycetes Sordariales Broad Neurospora crassa X04971 AF286411 XM_959004 XM_324476 Genome
216 Sordariomycetes Sordariales CBSC 15-5973 Sordaria fimicola AY545728 AY545724 DQ518175
51 Sordariomycetes Xylariales OSC 100004 Xylaria hypoxylon AY544692 AY544648 AY544760 DQ471114 DQ470878 DQ471042
1234 Taphrinomycetes Taphrinales CBS 356.35 Taphrina deformans DQ471024 DQ470973 FJ713610 DQ471170 DQ470927 DQ471097
265 Taphrinomycetes Taphrinales IAM 14515 Taphrina wiesneri AY548293 AY548292 AY548291 DQ471134 AY548298 DQ471134
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1voucher GB = obtained from GenBank, or genome databases without clear voucher numbers.

The phylogenetic analysis was run in RAxML v7.0.0 (Stamatakis 2006), partitioning by gene (six partitions) and estimating unique model parameters for each gene, as in Schoch et al. (2009). Models of evolution were evaluated as in Schoch et al. (2009) with the same models selected. For DNA sequences, this resulted in a general time reversible model (GTR) with a discrete gamma distribution composed of four rate classes plus an estimation of the proportion of invariable sites. The amino acid sequences were analysed with a RTREV model with similar accommodation of rate heterogeneity across sites and proportions of invariant sites. In addition, protein models for TEF1 and RPB2 incorporated a parameter to estimate amino acid frequencies. The tree shown in Fig. 1 was obtained by using an option in RAxML running a rapid bootstrap analysis and search for the best-scoring ML tree in one single run. This meant the GTRCAT model approximation was used, which does not produce likelihood values comparable to other programs. The full tree is shown here as Fig. 2 and was deposited in TreeBASE (www.treebase.org). We also ran 100 repetitions of RAxML under a gamma rate distribution option. The best scoring tree was included in TreeBASE.

Fig. 2.

Fig. 2

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A most likely tree obtained by RAxML for Ascomycota (as in Fig. 1). Phyla, subphyla, class, order and rankless taxa are indicated. Taxa designated as earth tongues are indicated in orange. The tree is displayed as two subtrees – orange arrows indicate where the subtrees were joined. The tree was rooted with outgroup Rhizopus oryzae (not shown). Bootstrap values are shown in orange above nodes and Bayesian posterior probabilities in blue below. Numbers were removed for nodes with 100 % bootstrap and 100 % posterior probability.

A second analysis was run using Bayesian inference of maximum likelihood in MrBayes v3.1.2 (Huelsenbeck & Ronquist 2001, Altekar et al. 2004) using models and parameters that were comparable to the maximum likelihood run. Data were similarly partitioned and amino acids were analysed, so that a mixture of models with fixed rate matrices for amino acid sequences could be evaluated. In all cases rate heterogeneity parameters were used by a discrete gamma distribution plus an estimation of the proportion of invariable sites. A metropolis coupled Markov Chain Monte Carlo analysis was run for 9 million generations sampling every 200th cycle, starting from a random tree and using 4 chains (three heated and one cold) under default settings. Two separate runs were confirmed to converge using Tracer v1.4.1 (http://tree.bio.ed.ac.uk/software/tracer/). The first 10 000 sampled trees (2 million generations) were removed as burn in each run. A 50 % majority rule consensus tree of 70 000 Bayesian likelihood trees from the two combined runs was subsequently constructed, and average branch lengths and posterior probabilities determined. The numbers of nodes shared with the most likely tree in Fig. 1 was determined and plotted on the branches. This tree was deposited in TreeBASE, along with the inclusive character set.

RESULTS

The phylogeny presented in Fig. 1 supports 15 classes (11 in Pezizomycotina, 1 in Saccharomycotina, 3 in Taphrinomycotina) with good statistical support (both ML bootstrap and Bayesian posterior probability) for 14. Phylogenies with all lineages in the analysed data matrix are included in Fig. 2. A run with 100 repetitions of RAxML under a gamma rate distribution option resulted in a best scoring tree with a log likelihood of -111983. This tree shared the same supported nodes with the one presented in Fig. 1 but had changes in poorly supported nodes regarding placement of the Eurotiomycetes and Dothideomycetes. The two Bayesian runs produced trees with harmonic means of likelihood values of -112094 and -112076, respectively, with similar topological differences in poorly supported nodes.

As can be seen in Fig. 1, we continue to find low bootstrap and posterior probability support for Leotiomycetes as a monophyletic clade using a combined analysis of protein and nucleic acids. In our analysis, this includes Neobulgaria pura as the earliest diverging lineage. The node internal from this lineage is found in all ML bootstrap trees, suggesting that this taxon is unstable in our analyses. No conflicts were detected in Neobulgaria genes under a previous study and missing data did not affect important nodes (Schoch et al. 2009). A repeat run under maximum likelihood was done with Neobulgaria pura removed under the same settings but with only 100 bootstrap repetitions. This trimmed dataset yielded a congruent phylogeny with increased bootstrap for Leotiomycetes (78 %; data not shown). The instability of the placement of Neobulgaria pura does not compromise any of the conclusions we present here and may be due to various reasons. Improved taxon sampling will likely help to resolve its placement in future analyses.

We find support for numerous backbone nodes in Ascomycota, as did Schoch et al. (2009). Our phylum-wide sampling of Ascomycota classes in this study, combined with the results of a previous study (Schoch et al. 2009), facilitated addressing the placement of the previously problematic and unsampled lineages such as the Geoglossaceae in relation to all currently accepted Ascomycota classes.

Taxonomy

Given their unique ascomatal development, ultrastructure of ascus apical apparatus, mossy habitat, and our multilocus gene phylogeny, Geoglossomycetes cl. & ord. nov. is justified here as incertae sedis in Pezizomycotina and ‘Leotiomyceta’.

Geoglossomycetes, Geoglossales Zheng Wang, C.L. Schoch & Spatafora, cl. & ord. nov. — MycoBank MB513351, MB513352

Ascomata solitaria vel gregaria, capitata, stipitata; stipe cylindricus, atrum, glabrum vel furfuraceus. Regio hymeniali capitata, clavata vel pileata, indistinctum ex stipite; hymenium atrum, continuatcum stipite ad praematuro incrementi grado. Asci clavati, inoperculati, octospori, poro parvo in iodo caerulescentes. Ascosporae elongatae, fuscae, pullae vel hyalinae, multiseptatae. Paraphyses filiformes, pullae vel hyalinae. Distributio generalis, terrestris, habitaile locus fere uliginoso et muscoso.

Type genus. Geoglossum Pers., Neues Mag. Bot. 1: 116. 1794; Geoglossaceae.

Ascomata scattered to gregarious, capitate, stipitate; stipe cylindrical, black, smooth to furfuraceous. Ascigerous portion capitate, club-shaped to pileate, indistinguishable from stipe. Hymenium surface black, continues with stipe at early development stage. Asci clavate, inoperculate, thin-walled, J+, usually 8-spored. Ascospores elongate, dark-brown, blackish to hyaline, septate when mature. Paraphyses filiform, blackish to hyaline. Global distribution, terrestrial, habitat usually boggy and mossy.

DISCUSSION

In keeping with the phylogeny presented in Fig. 1, we endorse use of the -myceta suffix in order to circumscribe well-supported clades above class. The numbers of these clades are limited, and the use of such taxa will continue to become more practical as our biological knowledge base broadens. Use of this suffix will also allow for the continued use of Leotiomyceta, a taxon that has already been defined with a Latin diagnosis provided as a ranked superclass (Eriksson & Winka 1997) and remains in use (Lumbsch et al. 2005, Wang et al. 2006a). We propose its continued use, but as a rankless taxon together with the newly proposed rankless taxa, ‘Saccharomyceta’, ‘Dothideomyceta’ and ‘Sordariomyceta’. Since these taxa are not currently accepted under the Code (McNeill et al. 2006), we will refrain from formal designations. The relevant clades are discussed below with the informal designations indicated in single quotations.

Subphylum Taphrinomycotina

As in recent studies using large multi-gene datasets (Spatafora et al. 2006, Sugiyama et al. 2006, Liu et al. 2009, Schoch et al. 2009), we find ML bootstrap support here for the monophyly of the Taphrinomycotina. The addition of sequences from protein coding genes has been vital to the establishment of statistical support for this grouping. Recent work has shown that the short generation times characteristic of species in this group make phylogenetic analyses particularly susceptible to long branch attraction artefacts (Liu et al. 2009). The placement of Neolecta in this subclade is also confirmed here. The club-shaped apothecia of the members of Neolecta share superficial similarity with those of the Geoglossaceae. Neolecta was long thought to be included in the Geoglossaceae until molecular work proved otherwise (Landvik 1996). In support of its placement in this early diverging group, Neolecta has several presumably ancestral features, such as simplified non-poricidal asci without croziers and the absence of paraphyses (Redhead 1979, Landvik et al. 2003). With additional sampling of both taxa and genes we find here moderate support for the monophyly of Taphrinomycotina, and thus demonstrate that the earliest diverging clade of the Ascomycota was dimorphic, with both filamentous and yeast growth forms. Nevertheless, it remains apparent that this part of the Ascomycota tree remains under sampled. This lack of adequate sampling is supported by the recent description of a clade labelled ‘Soil Clone Group I’ (SCGI). SCGI is ubiquitous in soil and is only known from environmental sequence data (Porter et al. 2008). It appears possible that they form a novel early diverging lineage outside of Taphrinomycotina. Very little remains known about their ecology, morphology and general biology.

Rankless taxon ‘Saccharomyceta’

‘Saccharomyceta’ includes the two remaining subphyla of Ascomycota, Saccharomycotina and Pezizomycotina. Saccharomycotina comprises the ‘true yeasts’ (e.g., Saccharomyces cerevisiae), although hyphal growth has been documented in some taxa (e.g., Eremothecium). The Pezizomycotina consists of the majority of filamentous, ascoma producing species, but numerous species are additionally capable of yeast and yeast-like growth phases. Thousands of species are only known to reproduce asexually. These two subphyla form a well-supported, monophyletic group that has been recovered in a large number of studies across a diversity of character and taxon sets. The recognition of ‘Saccharomyceta’ highlights the shared common ancestry of these two taxa and the inaccurate characterisation of Saccharomycotina as a primitive or basal lineage of the Ascomycota. Rather, its small genome size (Dujon et al. 2004) and dominant yeast growth phase can be characterized as derived traits for this subphylum.

Rankless taxon ‘Leotiomyceta’

We apply ‘Leotiomyceta’ as a rankless taxon containing the majority of fungi with a diversity of inoperculate asci (e.g., fissitunicate, poricidal, deliquescent). ‘Leotiomyceta’ excludes the earliest diverging classes of Pezizomycotina, Pezizomycetes and Orbiliomycetes. It was first defined as a superclass (Eriksson & Winka 1997). This definition has remained in use (Lumbsch et al. 2005, Spatafora et al. 2006). Included in this clade are the informal, rankless taxa ‘Dothideomyceta’, ‘Sordariomyceta’, as well as the classes Eurotiomycetes, Lecanoromycetes, Lichinomycetes, and a newly proposed class, Geoglossomycetes.

The type genus of Geoglossaceae, Geoglossum was initially proposed by Persoon (1794). Persoon described it as club-shaped, with unitunicate, inoperculate asci, with the type species given as Geoglossum glabrum Pers. Trichoglossum have historically been classified in Geoglossaceae, and Sarcoleotia has historically been classified in the Helotiaceae (Leotiomycetes). These inoperculate Discomycetes produce terrestrial, stipitate, clavate ascomata, commonly referred to as earth tongues, which include Leotia, Microglossum, Cudonia, and Spathularia. In terms of ascomatal development, species of Geoglossum, Trichoglossum, and Sarcoleotia possess a hymenium that freely develops towards the base, while other earth tongue fungi feature a distinct ridge to their hymenium, implying a developmental stage during which the hymenium is enclosed (Schumacher & Sivertsen 1987, Spooner 1987, Wang et al. 2006b). An enclosed hymenium has been observed as well in several other lineages, such as Cyttaria, Erysiphales and Rhytismatales in the Leotiomycetes (Korf 1983, Gargas et al. 1995, Johnston 2001). Although the name earth tongue implies these fungi are terrestrial and have no direct association found with other organisms, Trichoglossum, Geoglossum and Sarcoleotia globosa have often been recorded in boggy habitats abundant with bryophytes (Seaver 1951, Dennis 1968, Schumacher & Sivertsen 1987, Spooner 1987, Jumpponen et al. 1997, Zhuang 1998). Ascus apical morphology is one of the major features in distinguishing higher ascomycetes, and operculate ascomycetes as members of Pezizales have an apical or subapical operculum which is thrown back at spore discharge while a definite plug is present in the thickened ‘inoperculate’ ascus apex as in species of the Helotiales (Korf 1973). Ultrastructure of the ascus apical apparatus suggested no close relationship between Leotia lubrica and species of Geoglossum and Trichoglossum. A structure known as a tractus connects the uppermost spore to the apical wall and the spores to each other in Trichoglossum hirsutum, but is never found in other species of the Helotiales and is possibly homologous to structures in Sordariomycetes and Pezizomycetes (Verkley 1994). Recent molecular phylogenetic analyses (Sandnes 2006, Wang et al. 2006a, b) confirmed that the earth tongue fungi are not monophyletic. At least two origins occurred in Leotiomycetes: in Leotia and allies in Helotiales, and in Cudonia and allies in Rhytismatales. Geoglossum, Trichoglossum. Sarcoleotia (Geoglossomycetes as we define it) represent a third, independent lineage of earth tongues, which we confirmed does not belong within the Leotiomycetes.

DNA-only and combined model analyses produced conflicting placements of Geoglossaceae within Pezizomycotina. Previous analyses applying nucleotide sequences only placed the order as a sister group to the Lichinomycetes (Lutzoni et al. 2004, Spatafora et al. 2006), which includes a small number of lichenised species mainly associated with cyanobacteria (Reeb et al. 2004). Our sampling of Lichinomycetes includes two genera, Peltula and Lichinella that encompass at least some of the ascal diversity, i.e., rostrate and deliquescent, present in the class. In contrast, our combined amino acid and nucleotide model analyses resolved Geoglossaceae as an isolated, unique lineage of ‘Leotiomyceta’ with no supported sister relationship, in agreement with Schoch et al. (2009). Different levels of missing data underlie these two conflicting topologies, and several phenomena can potentially explain this conflict, ranging from model misspecification to long-branch attraction. Regardless of these concerns, our conclusion that the Geoglossaceae is a monophyletic lineage, unallied with members of the Leotiomycetes and any of the other large fungal classes remains strongly supported.

Eurotiomycetes and Lecanoromycetes are the two remaining classes in ‘Leotiomyceta’. Eurotiomycetes is arguably the most ecologically diverse class within Ascomycota including lichenised species, saprobes and pathogens of animals and plants. As currently defined, this class incorporates several distinct orders and three subclasses spanning virtually all known fungal ecological niches (Geiser et al. 2006). Lecanoromycetes contain the majority of the lichenised fungi (Miadlikowska et al. 2006). Earlier large-scale phylogenies (e.g. Lutzoni et al. 2004) have suggested a sister relationship between these two classes, but we find that such a relationship remains without strong statistical support (Fig. 1). Despite this, internal nodes are well supported enough to provide good support for the hypothesis that lichenisation evolved multiple times in the Ascomycota, with losses being rare (Gueidan et al. 2008, Schoch et al. 2009).

The remaining classes are discussed in relation to their respective rankless taxa listed below.

Rankless taxon ‘Dothideomyceta’

This taxon is well supported, with ML bootstrap of 91 % and a moderate Bayesian posterior probability of 92 %. It includes two classes of fungi which produce fissitunicate asci, Arthoniomycetes and Dothideomycetes. Arthoniomycetes consists of ± 1 600 species of lichenised and lichenicolous fungi with fissitunicate asci and exposed hymenia (Grube 1998, Ertz et al. 2009). Unlike other species with fissitunicate asci, these taxa have ascohymenial development, prompting their placement in a transitory group, or ‘Zwischengruppe’ that is intermediate between ascohymenial and ascolocular development (Henssen & Jahns 1974). The class is resolved as sister to Dothideomycetes, consistent with recent studies (Lutzoni et al. 2004, Spatafora et al. 2006, Wang et al. 2006a). Dothideomycetes is a large class containing two subclasses, Dothideomycetidae and Pleosporomycetidae (Schoch et al. 2006). Our analysis contains members of all known orders in the class, including recent additions (Boehm et al. 2009). This broad representation yields increased resolution in the placement of an order previously labelled incertae sedis, Botryosphaeriales (Schoch et al. 2006). Placement of Botryosphaeriales within subclass Pleosporomycetidae is well supported, as is a close relationship with the unplaced family Tubeufiaceae (Fig. 2).

Rankless taxon ‘Sordariomyceta’

‘Sordariomyceta’ contains three classes, Leotiomycetes, Laboulbeniomycetes and Sordariomycetes. We find similar resolution for this clade as for the ‘Dothideomyceta’. These three classes are characterised by the production of unitunicate, poricidal asci, or derivatives of such asci (e.g., deliquescent asci). Leotiomycetes and Sordariomycetes include numerous fungi associated with plants as pathogens, endophytes and epiphytes. The sordariomycete phylogeny is comparatively well resolved with 15 orders and 3 subclasses named (Zhang et al. 2006, Kirk et al. 2008). In contrast, the leotiomycete classification still poorly matches its inferred phylogeny. A recent class-wide effort to assess morphological and ecological data in a phylogenetic context continued to find high levels of diversity unaccounted for in the current classification (Wang et al. 2009). In addition to the aforementioned two classes, Fig. 1 also supports the placement of the Laboulbeniomycetes reported in Schoch et al. (2009) as part of a monophyletic lineage. The relationship between the Sordariomycetes and Laboulbeniomycetes is also well supported but we will refrain from naming this node until sampling can be expanded for the Laboulbeniomycetes. The class Laboulbeniomycetes encompasses an enigmatic lineage of insect symbionts and mycoparasites that have long proved problematic with respect to placement in higher-level classification schemes. Laboulbeniomycetes comprises two orders, Laboulbeniales and Pyxidiophorales, that are united by an ascospore synapomorphy of a darkened holdfast region and by molecular data (Weir & Blackwell 2001, 2005). Members of Pyxidiophorales possess globose perithecia with a single layer of wall cells, and long perithecial necks that release their ascospores passively in droplets at the tips of their necks; this mechanism is repeatedly derived within Ascomycota for insect dispersal of ascospores (Blackwell 1994). For this reason, they have been likened to other insect-dispersed perithecial ascomycetes (e.g., Ophiostomatales) that now are strongly supported as members of Sordariomycetes. Laboulbeniales includes ectoparasites of insects and displays morphological traits not found elsewhere in the Ascomycota. They form apomorphic ascomata produced by the division and enlargement of ascospores that are difficult to characterize in existing ascomatal terms. Laboulbeniales feature an ostiole, however, which is consistent with perithecia produced by hyphal growth. Determinate growth of the ascospore with a series of predictable cell divisions produces a thallus of a finite number of cells that is characteristic at the genus and species level (Tavares 1979). The analyses presented here strongly support Laboulbeniomycetes as sister to Sordariomycetes. This placement corresponds with the terminology originally applied to this group (Thaxter 1896). It is interesting to note that while species of Pyxidiophorales are endowed with a diverse group of anamorphs, members of Laboulbeniales are mainly known to reproduce sexually.

Summary

In conclusion, we propose two monotypic formal taxa and describe continued support for four informal rankless taxa. Important improvements in the resolution of deep nodes within the Ascomycota may be attributed to multi-gene sequence data produced by AFTOL and other projects during the last 5 years. The accelerating accumulation of genome-scale sequence data will continue to challenge and improve existing phylogenetic hypotheses. However, in order to direct limited resources towards under-sampled areas in the fungal phylogeny, an accurate, up-to-date classification is required. By placing three earth tongue genera in a separate newly described class, we underscore and communicate the genetic diversity that is found in the fungi producing these very convergent morphologies.

Acknowledgments

We are grateful to Kentaro Hosaka, Dan Luoma and Zhuliang Yang for the photographs used. We acknowledge funding provided by NSF through a grant (DEB 0717476) to J.W.S. and C.L.S. (while at Oregon State). C.L.S. was also supported in part by the Intramural Research program of the National Institutes of Health. Z.W. was supported by the Yale University Anonymous Postdoctoral Fellowship.

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