“Grassland” Sparrow Clade

Ornithology Program (HRC) Harry Reid Center for Environmental Studies

4-2007

A molecular evaluation of the North American “Grassland” sparrow clade

John Klicka University of Nevada, Las Vegas, [email protected]

Garth M. Spellman University of Nevada, Las Vegas, [email protected]

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Repository Citation Klicka, J., Spellman, G. M. (2007). A molecular evaluation of the North American “Grassland” sparrow clade. Auk, 124(2), 537-551. Available at: https://digitalscholarship.unlv.edu/hrc_ornithology/24

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A MOLECULAR EVALUATION OF THE NORTH AMERICAN “GRASSLAND” SPARROW CLADE John Klicka1 and Garth M. Spellman

Barrick Museum of Natural History, Box 454012, University of Nevada Las Vegas, 4505 Maryland Parkway, Las Vegas, Nevada 89154, USA

Abstract.—Because they share several morphological and ecological characters, the North American sparrow (Emberizidae) genera Ammodramus, Passerculus, and Xenospiza have historically been considered members of a well-defi ned “grassland” sparrow assemblage. Relationships among the 11 members of this group have been the subject of much taxonomic debate, yet no comprehensive molecular assessment of relationships has been done. We investigated these relationships using mitochondrial DNA sequence data that included complete cytochrome-b and ND2 genes. Phylogenetic reconstructions derived via parsimony, likelihood, and Bayesian methods were congruent. The grassland sparrows, as presently confi g- ured, are polyphyletic. Pooecetes gramineus, Amphispiza belli (but not A. quinquestriata and A. bilineata), Oriturus superciliosus, and all three species of Melospiza are included in a reconfi gured clade, whereas the traditional forms of Ammodramus savannarum, humeralis, and aurifons are placed well outside of these. Within the clade of interest, Ammodramus remains polyphyletic, with leconteii, maritimus, nelsoni, and caudacutus forming a well-resolved clade apart from henslowii and bairdii. The la er are in another strongly supported clade that also includes Passerculus and a Xenospiza– Melozpiza sister pairing. Pooecetes, Amphispiza (belli), and Oriturus represent early lineages in this clade that today have no close living relatives. The polyphyly of the genus Ammodramus is likely the result of morphological convergence a ributable to similar adaptive responses to the occupation of similar habitats. In general, the morphological and ecological factors that have defi ned the grassland sparrows are poor indicators of relatedness. Taxonomic revisions are suggested. Received 8 December 2005, accepted 3 May 2006.

Key words: Emberizidae, grassland sparrow clade, Mexican endemics, mitochondrial DNA, molecular systematics, Oriturus, sparrows, Xenozpiza.

Evaluación Molecular del Clado de Gorriones de Pastizales de Norte América

Resmen.—Debido a que comparten varios rasgos morfológicos y ecológicos, los géneros norteamericanos Ammodramus, Passerculus y Xenospiza (Emberizidae) se han considerado históricamente como miembros de un ensamblaje bien deﬁ nido de gorriones de pastizales. Las relaciones entre los 11 miembros de este grupo han sido objeto de muchos debates taxonómicos, pero no se ha hecho ninguna evaluación exhaustiva de sus relaciones con base en datos moleculares. Investigamos las relaciones entre estas aves utlizando datos de secuencias mitocondriales completas de los genes citocromo b y ND2. Las reconstrucciones ﬁ logenéticas basadas en métodos de parsimonia, verosimilitud y Bayesianos fueron congruentes. El grupo de los gorriones de pastizales tal como está

1E-mail:[email protected] 537 538 Klicka and Spellman [Auk, Vol. 124

confi gurado actualmente es polifi lético. Pooecetes gramineus, Amphispiza belli (pero no A. quinquestriata ni A. bilineata), Oriturus superciliosus y las tres especies de Melospiza están incluidas en un clado reconfi gurado, mientras que las formas tradicionales de Ammodramus savannarum, humeralis y aurifons se ubican bien afuera de las demás. Dentro del clado de interés, Ammodramus es aún polifi lético, con leconteii, maritimus, nelsoni y caudacutus formando un clado bien resuelto, aparte de henslowii y bairdii. Estos dos últimos taxones están en otro clado fuertemente respaldado que también incluye a Passerculus y la pareja de taxones hermanos Xenospiza–Melozpiza. Pooecetes, Amphispiza (belli) y Oriturus representan linajes que se separaron tempranamente dentro de este clado y en la actualidad no tienen parientes cercanos. La polifi lia del género Ammodramus probablemente se debe a convergencia atribuible a respuestas adaptativas similares a la ocupación de ambientes similares. En general, los factores morfológicos y ecológicos que han defi nido a los gorriones de pastizales son malos indicadores de las relaciones de parentesco. Se sugieren revisiones taxonómicas.

Many of the temperate-zone sparrows of Chapman 1895) until it was raised to generic North America have been divided into one of status by Ridgway (1901), where it has remained two traditional groups, the “grassland” and the (but see Paynter and Storer 1970). Xenospiza, the “brushland” nesting sparrows (e.g., Paynter montane Mexican endemic fi rst described by 1964, Dickerman et al. 1967, Robins and Schnell Bangs (1931), is a relatively recent addition 1971). The former comprises the modern gen- to the group. Although most workers place era Ammodramus, Passerculus, and Xenospiza, it among the grassland sparrow assemblage whereas the la er includes Melospiza, Passerella, (Dickerman et al. 1967, Robins and Schnell 1971; Zonotrichia, and Junco. Although formal phyloge- but see Pitelka 1947), its “exact position within netic analyses were lacking historically, members this group is less obvious” (Dickerman et al. in each of these complexes were assumed to be 1967). The group, as currently confi gured, com- closely related through “recency of common prises 11 recognized (i.e., “biological”) species. ancestry” (Robins and Schnell 1971). Several It has been the focus of some formal systematic additional North American genera not assigned analyses, including a thorough phenetic analysis to one of these core “clades” include Aimophila, by Robins and Schnell (1971), who subdivided Oriturus, Spizella, Pooecetes, Chondestes, and the complex into two clades, Ammodramus (the Amphispiza. These taxa are typically listed before grassland sparrows, including the currently (American Ornithologists’ Union [AOU] 1998) or recognized forms sandwichensis, aurifrons, hume- a er (Paynter and Storer 1970, Sibley and Monroe ralis, savannarum, and bairdii) and Ammospiza 1990) the grassland and brushland assemblages (the “marshland” sparrows, which included the in modern linear taxonomies, and their system- modern leconteii, caudacuta, nelsoni, maritimus, atic affi nities remain poorly understood. henslowii, and X. baileyi). Zink and Avise (1990) Although the “grassland” sparrow clade studied relationships among most members of appears to be well circumscribed, li le agree- the group (Xenospiza lacking) using allozyme ment exists regarding relationships among its and mitochondrial RFLP (restriction fragment constituents (the numerous taxonomic revi- length polymorphism) data. Both data sets iden- sions a empted for this group of sparrows tifi ed a maritimus–caudacutus–nelson–leconteii are reviewed by Murray [1968]). The genus clade and a probable henslowii–bairdii sister Ammodramus, in particular, has a tumultuous relationship. The allozyme evidence suggested taxonomic history, with its nine current mem- a genetically distinct group consisting of savan- bers historically divided into anywhere from narum and the South American forms humeralis one (AOU 1998) to four (Ridgway 1901) to and aurifrons, but their placement within the seven (Oberholser 1917) diff erent genera (Table ingroup was equivocal. They concluded that the 1). Early taxonomies also listed Passerculus as genus Ammodramus may not be monophyletic a member of Ammodramus (e.g., AOU 1886, and that additional analyses using more distant April 2007] Grassland Sparrow Systematics 539

outgroups are required. Here, we undertake y ] is the . ]

f such analyses. ible o A thorough systematic revision requires that edition part

all members of the clade of interest be identiﬁ ed. b 1971, S be In addition to “known” ingroup taxa, genera to

. (1998) with uncertain taxonomic aﬃ nities should be chnell ent S examined, as well as those taxa linked with ears qu and

members of the ingroup by earlier taxonomies. bse considered u

s Because closely related taxa provide the optimal y

120 y obins Ammodramus humeralis Ammodramus aurifrons outgroups for rooting trees (Wheeler 1990, Smith [ Ammodramus bairdii [ the

past or

1994), these, too, need to be identiﬁ ed. In short, f

1970, R a modern phylogenetic hypothesis of generic the not

traditionall

t u

relationships among all New World sparrows er

torer

] b

not v ]

o is required, and such a hypothesis does not yet

list ere -

and exist. A few, less complete, systematic studies on

w higher-level sparrow relationships have been times check nter and

y s e

a done. Pa en and Fugate (1998) used morpho- v u

1957 logical, behavioral, oological, and allozymic abo

.g., P ario e the

characters to investigate systematic relation- ( v or f

listed ships among “the emberizid sparrows.” They at Myospiza humeralis Myospiza aurifrons

e [ g thors x examined 18 genera, all from Paynter’s (Paynter u a era

v and Storer 1970) “ﬁ rst group” and considered by co onomists f

most Paynter to represent the “typical” emberizines. x o

comple

] [ y ta ]

b Most of the characters used in that work were

w the

scope the same as those used to originally describe the

y ears b

y genera under investigation. Not surprisingly, the

1917 AOU 1957 AOU 1998 sparro

many traditional taxonomic groupings were ond recent y treated

recovered, including a grassland sparrow clade be in

not comprising Xenospiza baileyi, Passerculus san-

as w berholser ere wichensis, Ammodramus savannarum, A. henslowii, rassland Myospiza humeralis Myospiza aurifrons [ [ ico w g

x and A. bairdii. By contrast, Carson and Spicer e

the (2003) used modern molecular methods to birds

f Ammodramus

o investigate sparrow relationships. Their results

into these

1931). M ] identiﬁ ed a well-supported clade that contained , ] s g ed

g some members of the grassland sparrow com- an tion

u plex, including P. sandwichensis, A. leconteii, and mer

members

f A. henslowii but also all members of the putative o . 1931 (B distrib been

) brushland sparrow genus, Melospiza. Placed as in

e v ed

clade sister to this assemblage was an Amphizpiza belli– g ha w ) Pooecetes pairing. Their unusual result suggests merican A Myospiza humeralis Myospiza aurifrons

described a taxonomic arrangement that diﬀ ers consider- [ [

abrid th sparro

u (

rst ably from that found in recent classiﬁ cations o

ﬁ S , (e.g., Sibley and Monroe 1990, AOU 1998).

their The goals of the present study are twofold. rassland

f a g o

] First, the work of Carson and Spicer (2003) endemic humeralis, aurifrons ]

treatment se

(

u is extended to include additional unsampled ican eca x

merican genera, with the goal of conclusively identi- e A species

M fying all members of the grassland sparrow a onomic

x orth is

clade. Second, once ingroup membership is a 1990). B

y N established, we will focus on discerning rela- el Myospiza

v onroe tionships within the clade. Given the checkered si he u M Xenospiza T

Myospiza aurifrons Myospiza humeralis

a b taxonomic history of this group (Table 1), a cl x and e Table 1. T Table [ AOU 1886, 1895 AOU 1910 O Ammodramus sandwichensis sandwichensis Passerculus Ammodramus savannarum Ammodramus bairdii sandwichensis Passerculus Ammodramus savannarum sandwichensis Passerculus Ammodramus henslowii Coturniculus savannarum Ammodramus leconteii sandwichens Passerculus Ammodramus savannarum Ammodramus savannarum henslowii Passerherbulus Ammodramus bairdii Ammodramus caudacutus leconteii Passerherbulus Ammodramus maritimus Nemospiza henslowii [ caudacutus Passerherbulus bairdii Cetronyx Ammospiza caudacutus leconteii Passerherbulus maritimus Passerherbuulus henslowii Passerherbulus Thryospiza maritimus caudacutus Passerherbulus Ammospiza caudacutus Ammodramus henslowii Ammdramus leconteii Ammospiza maritima Ammodramus bairdii Ammodramus caudacutus nelsoni Passerhebulus Ammodramus maritimus nelsoni Ammodramus deﬁ nitive revision is warranted. Xenospiza baileyi 540 Klicka and Spellman [Auk, Vol. 124

Materials and Methods Massachuse s) purifi cation following the manufacturer’s protocols. Standard, 20-µL sequencing Sampling strategy.—All 11 currently recog- reactions were performed using 4 µL of BigDye nized members (Sibley and Monroe 1990) of (Applied Biosystems, Foster City, California) the traditional grassland sparrow assemblage and 20–40 ng of purifi ed and concentrated PCR were included in this work. To ensure that no product. Products of these reactions were puri- potential ingroup members were omi ed, we fi ed using a magnetic-bead clean-up procedure also examined at least one representative of designed by Agencourt Bioscience (Beverly, each additional, currently recognized (Sibley Massachuse s) and run on an ABI 3100-Avant and Monroe 1990) sparrow genus, excepting the automated sequencer. Complementary strands monotypic Cuban form Torreornis. Analyses of of each gene were unambiguously aligned these preliminary data (J. Klicka unpubl. data) using SEQUENCHER, version 4.2 (Gene Codes identifi ed a well-supported clade that included Corporation, Ann Arbor, Michigan). The verac- all genera traditionally considered members of ity of the sequence data was supported in sev- the grassland sparrow assemblage but also rep- eral ways. Both light and heavy strands were resentatives of the following additional genera: sequenced for all PCR fragments. No gaps, Oriturus, Pooecetes, Amphispiza, and Melospiza. insertions, or deletions were apparent in the Subsequently, all these taxa were considered a aligned sequences, and all data translated (using part of the ingroup for the present study. The MEGA, version 3.01; Kumar et al. 2004) correctly preliminary analysis also identifi ed a well- into amino acid form. The resulting sequences supported sister clade from which appropri- include the complete cyt-b (1,143 base pairs [bp]) ate outgroups were chosen. The six outgroup and ND2 (1,038 bp) genes for a total of 2,181 bp taxa selected each represent a subclade within of concatenated data. this larger sister clade. Complete ingroup and Phylogenetic protocols.—Phylogenetic analy- outgroup species representation is provided in ses were preceded by data exploration. Using Table 2. PAUP*, version 4.0b4a (Swoff ord 2000), we con- Laboratory protocols.—Total genomic DNA structed genetic-distance matrices using both was extracted from all specimens using a inter- and intrageneric pairwise comparisons. DNeasy tissue-extraction kit (Qiagen, Valencia, The relatively low genetic distances uncovered California), following the manufacturer’s pro- suggested limited potential problems a ribut- tocol. We amplifi ed the mitochondrial DNA able to homoplasy. Nevertheless, we plo ed (mtDNA) cytochrome-b (cyt-b) gene using the pairwise comparisons of uncorrected genetic primers L14764 (Sorenson et al. 1999) and H4A distances for each gene and gene partition (i.e., (Harshman 1996), and the NADH dehydroge- codon position) for all ingroup taxa to assess nase subunit 2 (ND2) gene using L5215 (Hacke the degree of possible “saturation” eff ects. The 1996) and H6313 (Johnson and Sorenson 1998). evolutionary dynamics of each gene and gene Because the X. baileyi sample was obtained from partition were also investigated for all ingroup a study skin, DNA extraction and polymerase taxa. Parameters examined include transition: chain reaction (PCR) preparation were per- transversion ratio (Ts:Tv), relative rates of formed in a separate laboratory where no pre- evolution, nucleotide composition (%), and the vious avian genetic work had been conducted. gamma-shape parameter (α). Potential nucleo- Amplifi cations of Xenospiza divided each gene tide composition bias was assessed by perform- into two fragments using internal primers: L ing a series of chi-square tests of homogeneity 5758 and H5766 (Sorenson et al. 1999) for ND2 on the informative data of each gene and gene and LCBOB and H15299 (Klicka et al. 2001) for partition. For each gene, we also plo ed the cyt-b. For all fragments, amplifi cations were relative proportions of each nucleotide for each done in 12.5-µL reactions under the following taxon used (e.g., C vs. T and A vs. G). Outliers conditions: denaturation at 94°C, followed by 40 in such plots likely indicate taxa that are prob- cycles of 94°C for 30 s, 54°C for 45 s, and 72°C for lematic with respect to nucleotide composition 1 min. This was followed by a 10-min extension biases. To ensure that the data sets for each at 72°C and a 4°C soak. Products were purifi ed gene contained congruent phylogenetic signal, using a Qiaquick PCR purifi cation kit (Qiagen) we executed a partition homogeneity test (the or ExoSAP-IT (USB Corporation, Cambridge, incongruence length diff erence test [ILD] of April 2007] Grassland Sparrow Systematics 541

y, these

istor h , ND2) H ug b - ral t u y; LSUMNS = y ltho at c ( . A f N p istor o u

H ro m ral u g u mbers se u at this n f

Mu f N o o .

y d m ank DQ459521, DQ459541 DQ459511, DQ459531 u u date arrick B

st se

B en later inal Mu

orie j g ar ield ori this

1994 DQ459514, DQ459534 at

their

data in

1985 DQ459516, DQ459536 ctober 1994 DQ459513, DQ459533 1994 DQ459508, DQ458528 cher y; FMNH = F gy; MBM = M pril y 1997 DQ459515, DQ459535 y 1997 DQ459522, DQ459542 u 1994 DQ459512, DQ459532 l l ne ne o (1990) 1994 DQ459523, DQ459543 v ne istor y, 9 O y, oolo ise or ne H Z nt y, 4 A 4 y, y Av u ral nt o y, 12 Ju y, y, 12 Ju y, u y, 19 Ju y, y, 19 Ju y, y, 9 Ju y, u and at y 2002 DQ459517, DQ459537

. nt nt C o nt nt localit nt

u u ar u u ertebrate f N y, 22 Ju y, ink u C o o o 1996 DQ459524, DQ459544 o o u

ton o o nt f V g m y Z g o u an

ctions C b u 1963 DQ459509, DQ459529 u C u C

u C u C ie o m u se u C y 1990 DQ459506, DQ459526 D sed ember pril se ashin appropriate , 20 J itkin u v Mu osea osea

G ar an o o hotea hotea ake u ell g the , R , W , A , R

y 1999 DQ459525, DQ459545 , S B , 6 A , 6 y, Mu 1999 DQ459518, DQ459538 l those an , L , C , C date reconstr

ide g ord v y 1989 DQ459510, DQ459530 , 19 N pril F , 8 J DQ459507, DQ459527 DQ459507, a erkele ornia and pro f altenan

ederal , 20 Ju amon , B

z y ose ose innesota ontana ontana innesota ontana innesota innesota , M to enetic ames man

ali F g J J et u , 13 A , 13 rom c lo : M : M : M : M : M : C : M : M ornia f able an an opan f

y : Qu as ali localit are orelos : S : S istrito : Tu : C ph alisco w g

tates tates tates tates tates tates tates tates f C ica ica : BMNH = J o : D : M : J ras in S S S S S S S S

y x DS x u R R ico ico ico entina neither x x x atemala sed preﬁ ersit g iations

e e e ond y, nited nited nited nited r nited nited nited nited v osta ollectin osta v u d ni the u

st bbre

ith r u w o y. A

d or u C f a ; MVZ = U

specimens f samples rce

97-38) U 94-84) U 94-063) U 94-41) U 97-33) U u cience k k k k k samples S present so

” ” ” ” ral the u

DNA DNA at in

mt localities

f N Ammodramus ample

sed o BMNH (X7370) U BMNH (X7309) U “DS-54 “DS-57

u he m u riﬁ and . T

u se as g e FMNH (343328) M (343328) FMNH ltrap BMNH (j BMNH V y Mu dates LSUMNS B-9941 C B-9941 LSUMNS u specimens BMNH (j BMNH

as MBM#6640 H g LSUMNS B-16232 C B-16232 LSUMNS or L ersit f BMNH#23380 M BMNH#23380 ided MVZ (FC20306) U (FC20306) MVZ v v ada ni “DS-9” DQ459519, DQ459539 v rces “DS-46” DQ459520, DQ459540 uralis e MBM#6460 A MBM#6460 U pro u Ĵ BMNH (j BMNH y BMNH (j BMNH MBM#10538 Gu MBM#10538 so ollectin

f N FMNH (343329) M (343329) FMNH BMNH (j BMNH tate o m S y u kindl S

se ersit on isiana v Mu x u a thors ni a o u M. melodia M. lincolnii Passerculus sandwichensis Passerculus Xenospiza baileyi Oriturus superciliosus Melospiza georgiana Melospiza georgiana A. bairdii Pezopetes capitalis Atlapetes gu A. citrinellus Pipilo ocai M. leucotis Table 2. C Table T A. maritimus A. henslowii Pooecetes gramineus Pselliophorus tibialis Amphispiza belli A. caudacutus A. nelsoni U Ammodramus lecontei L a 542 Klicka and Spellman [Auk, Vol. 124

Farris et al. 1995) in PAUP*. This test consisted was then implemented using the TVM + I + Γ of 100 replicates and considered only informa- and TrN + I + Γ models of sequence evolution tive characters (Cunningham 1997). Given that for the respective cyt-b and ND2 partitions. no signifi cant diff erences were identifi ed (P = Specifi c nucleotide-substitution model param- 1.00), we combined the data for all analyses. eters were le undefi ned and estimated as part We performed phylogenetic analyses of the analysis. All Bayesian analyses were initi- using both maximum-parsimony (MP) and ated from random starting trees. Four Markov- maximum-likelihood (ML) approaches. We con- chain Monte Carlo chains were run for 1 million ducted both weighted and equal-weighted par- generations and sampled every 100 genera- simony analyses. In the former, transitions were tions, yielding 10,000 trees. The fi rst 100,000 downweighted in relation to transversions by generations (= 1,000 trees) were discarded to one-third for both genes. Support for individual ensure that chain stationarity had been reached. nodes was assessed using MP heuristic boot- To ensure that the Markov chain was sampling strap (Felsenstein 1985) with 500 pseudorepli- from the posterior distribution, this procedure cates, each with 10 random-addition sequence was repeated two more times. Because all three replicates. We used MODELTEST, version 3.04 runs converged on the same distribution, all (Posada and Crandall 1998), to select the most trees (excluding those sampled before burn-in) appropriate model of sequence evolution for were combined, yielding a total of 27,000 topol- ML analyses. Akaike’s Information Criterion ogies from which a 50% majority-rule consensus (AIC) was used (see Posada and Buckley 2004) tree was reconstructed. Nodes having posterior to identify the GTR + I + Γ model as the best probability values of 95% or greater on this tree fi t to our combined data. We obtained an ML were deemed signifi cantly supported. estimate of phylogeny using PAUP* (Swoff ord 2000) with parameter se ings as determined by Reslts MODELTEST. Node support for ML analyses was determined via bootstrapping (Felsenstein Sequence characteristics.—As expected, the 1985), with 100 pseudoreplicates and full heu- ND2 gene was slightly more variable than ristic searches using random addition of taxa. cyt-b (Table 3). Over the 2,181 bp of combined For both MP and ML bootstrap analyses, we sequence, 610 (28%) sites were variable and, of considered values of >70% to indicate good these, 363 (16.6%) were potentially phylogeneti- node support. It is well understood that one cally informative. Overall, slightly more than of the shortcomings of MP is its inability to 47% of third-position sites varied. All plots of detect homoplasy on long branches, a poten- genetic distances (not shown) were linear, indi- tial source of bias in phylogeny estimation cating that homoplasy is relatively low. In birds, (Felsenstein 1978, Swoff ord et al. 1996). Because cyt b approaches saturation between 8% and 9% the model chosen is more resistant to error divergence (Griffi ths 1997). For our data, uncor- caused by homoplasy (Kuhner and Felsenstein rected cyt-b ingroup distances ranged from 1% 1994, Huelsenbeck 1995), we decided a priori to (A. nelsoni–A. caudacutus) to 7.9% (A. maritimus– consider our likelihood topology as our best M. lincolnii) divergent, with a mean diff erence of estimate of a phylogenetic hypothesis for the 6.3% (Table 4). Corresponding values from ND2 grassland sparrow assemblage. distances are greater in all comparisons, rang- Bayesian inference (Rannala and Yang 1996) ing from 2% (A. nelsoni–A. caudacutus) to 13.2% was used primarily as a means of assessing (A. belli–M. georgiana), with an average of 10.8%. support for nodes obtained via other (ML, MP) This la er value is approaching the known satu- tree-building methods. Because the use of a ration point of the ND2 gene (10–12% [Hacke single evolutionary model with data composed 1996], 12–13% [Johnson and Sorenson 1998]). of diff erently evolving subsets may result in Nucleotide composition and bias varies mismodeling and signifi cant systematic error slightly between these two genes; both display a (Brandley et al. 2005), we partitioned our data defi ciency of guanine and an excess of cytosine by gene (cyt b and ND2) and ran each indepen- nucleotides. Base composition biases (Table 3) dently through MODELTEST to determine the recovered are similar to those reported from AIC best-fi t model. The program MRBAYES, other avian studies. Tests of homogeneity of version 3.1 (Huelsenbeck and Ronquist 2001) base frequencies across ingroup taxa were not April 2007] Grassland Sparrow Systematics 543

signiﬁ cant for both genes combined (χ = 8.57, . is

on df = 57, P = 1.00), each individual gene, or any

gene (codon) partition (Table 3). Codon-position- α cted

∞ speciﬁ c, gamma-shape parameter (α) estimates u partition indicate that among-site rate heterogeneity is a likely problem in this data set. The problem is each composition

:Tv :Tv

reconstr most acute at second-position sites where values s or

es for both genes (cyt-b = 0.009, ND2 = 0.013) lie y f base

g sl outside the range (0.1–0.5; Yang 1996) typical of u

ean gamma-shape parameter estimates. chan T f 2

. M Phylogenetic analyses.—Interpreting the results o

ltaneo χ a x u = 1.000 = 1.000 = 0.976 7.3 9.9 9.5 0.128 0.013 = 1.000 10.0 0.221 = 1.000 = 1.000 = 1.000 9.2 6.7 6.8 0.115 0.138 0.009 = 0.999 19.7 0.839 of alternative phylogenetic methods is straight- ta P P P P P P P P forward, because the weighted MP, ML, and sim mber p

u u Bayesian topologies were identical (Fig. 1). All n

ro e

g methods support a Melospiza–Xenospiza sister g in

relationship. Ammodramus is clearly shown to era v all estimated be polyphyletic, with its members distributed

or among three clades. Ammodramus bairdii and A. ere f the

henslowii are embedded within a well-supported w es

are clade that also contains Passerculus, Xenospiza, enes

u al es and Melospiza. A separate, well-deﬁ ned clade u v comprises the forms leconteii, caudacutus, nel- al α

ND2 g soni, and maritimus. The remaining members

and of Ammodramus (savannarum, humeralis, auri- :Tv) v :Tv) and s

b frons) are only distantly related to the present :Tv :Tv - s (T

T clade and are instead most closely linked with

he members of the genus Arremonops (J. Klicka ratio

. T unpubl. data). Amphispiza belli is placed among ht tochrome

g the grassland sparrows as sister (though sup- y c

ersion ei

e port is lacking) to the monotypic form Pooecetes. v (%) A C (%) G (%) T (%) v w

the The genus Amphispiza is thus rendered poly- al f rate o trans elati phyletic, given that its congeners (bilineata and : qu

e quinquestriata; Sibley and Monroe 1990) have g

e R

in strong aﬃ nities elsewhere in the emberizid v v en namics phylogeny, closest to the monotypic forms g y ha ransition

d lo

Chondestes and Calamospiza (J. Klicka unpubl. y c

ormati h f

sites data). This relationship was also suggested by

in Carson and Spicer (2003). The obscure Mexican all

P speciﬁ

- endemic Oriturus is placed within the grassland

ith g PAUP*. T g PAUP*. sparrows, but its taxonomic aﬃ nities within the w sin sites

ariable clade are uncertain. It likely represents a relict u

position lineage with no close, extant “relatives.” - Bayesian posterior probabilities have been V ences

obtained criticized as too liberal (Suzuki et al. 2002) qu codon ies

se 346 71 37 7.8 36.6 30.3 15.8 17.3 sites g mber and prone to a high type-1 error rate (Erixon

f o all et al. 2003; but see Wilcox et al. 2002, Alfaro and

er et al. 2003), whereas nonparametric bootstrap- topolo v

b o erall o

ping proportions are known as conservative w t ed estimates of phylogenetic accuracy (Hillis and

g f

o Bull 1993). In the present study, nodes identiﬁ ed 346 36 15 4.0 16.5 33.6 9.9 39.9 9.9 33.6 16.5 4.0 15 36 346 6 10 1.0 381 20.6 25.1 12.7 41.6

346 245 172 27.0 37.5 44.3 5.7 12.5 5.7 44.3 37.5 27.0 172 245 346 381 212 117 21.2 34.2 53.8 3.2 8.8 30.2 36.1 10.3 23.3 354 224 1,038 13.0 1,143 10.0 26.9 36.6 13.0 23.6 256 139

34 381 16 3.4 25.8 30.8 23.1 20.3 era ll ll v nd rd st st nd rd as well supported via each of these methods are tochrome one a

osition in complete agreement. Eight of 13 ingroup Table 3. Ov Table A 2 3 Cy 1 A 1 2 3 ND2 Nu P nodes (Fig. 1) have posterior probabilities of 544 Klicka and Spellman [Auk, Vol. 124

le g sin

a g ieldin , y ed g era v a

been

e v ha

ps u ro g t u o

he . T enes w) g belo ND2 ( and ) e v abo w). ( b - belo 1, mn tochrome u y c

col 12.14 12.10 10.12 8.86 12.14 9.92 10.02 11.27 8.57 ( the

or (%) f 8.01 6.91 5.16 6.92 comparisons

8.45 7.17 5.51 7.01 5.60 5.95 5.95 6.39 7.09 p ences 8.32 6.74 g u 7.98 er ro v g 6.48 5.77 8.06 6.47 4.99 7.41 5.95 7.41 6.74 5.69 6.83 7.09 6.04 7.35 7.26 8.14 di in

3.85 8.59 6.39 6.74 7.45 7.35 6.65 6.30 6.39 6.91 7.17 7.09 3.32 3.85 8.55 6.91 7.26 7.10 7.35 7.00 6.30 7.09 7.87 7.17 4.72 5.69 6.83 5.95 8.61 6.82 ise 4.11 2.89 7.19 5.86 6.91 4.90 8.55 6.47 6.91 7.26 6.82 8.65 7.00 6.56 6.92 7.35 6.21 6.74 w 2.89 0.96 3.85 8.44 6.47 6.82 7.54 7.44 6.56 6.21 6.82 7.26 7.26 7.17 5.34 5.51 5.95 7.90 6.65 4.37 6.92 5.34 5.42 5.42 14 13 12 11 10 4 5 6 7 8 9 1 2 3 pair

ncorrected on or x f a e A. caudacutus A. maritimus A. nelsoni M. lincolnii Amphispiza belli Ammodramus henslowii A. bairdii M. georgiana Melospiza melodia Passerculus sandwichensis Passerculus Pooecetes gramineus Xenospiza baileyi Oriturus superciliosus u al A. leconteii A. v 12 12.85 13 14 15 12.40 10.79 10.69 12.49 11.56 10.89 11.46 11.27 11.95 10.89 13.74 11.85 11.27 12.97 12.33 11.85 6.94 12.24 12.91 13.01 12.04 13.01 10.50 10.60 11.62 11.27 11.18 11.37 5.49 11.27 11.75 5.49 11.75 10.89 13.44 11.66 11.56 12.39 5.78 12.43 12.24 12.04 6.65 12.33 12.81 2.02 12.521 2.14 10 11 11.46 9.54 9.73 9.92 11.13 9.92 8.48 11.27 12.97 11.85 11.56 12.49 12.81 12.43 13.20 12.62 12.93 8 9 13.76 11.75 7.23 12.10 10.12 5.68 5.68 4.43 13.99 12.14 7.80 11.81 10.79 7 13.47 11.75 7.51 12.39 10.69 Table 4. U Table 6 13.23 11.56 10.12 12.20 5 13.75 12.78 11.62 3 4 13.90 13.18 11.46 T 2 April 2007] Grassland Sparrow Systematics 545

Fig. 1. Phylogenetic hypothesis for the “grassland” sparrows as determined by weighted parsimony, maximum likelihood, and Bayesian methods. Branch lengths reflect likelihood estimates (GTR + I + Γ model of evolution, I = 0.5831, α = 2.2334; –Ln length = 10,910.2456). Nonparametric bootstrap support as determined via likelihood and parsimony methods are indicated above and below (respectively) the nodes. Bold lines indicate significant (>95%) Bayesian posterior support values.

≥95% and ML and MP bootstrap proportions member of the genus Amphispiza (belli), and the of ≥70%. No nodes are supported by one confi - monotypic forms Pooecetes and Oriturus. The dence estimate but not the others. This consen- clade recovered was not expected; this particu- sus gives us a high degree of confi dence in those lar taxon assemblage had not been predicted in supported portions of the tree and, overall, we any previous taxonomy. Relationships within submit that Figure 1 is our best estimate of phy- the historically problematic genus Ammodramus logenetic relationships for this sparrow clade. are resolved here, as is the debate concerning However, caution should be used in interpret- the systematic position of Xenospiza. We identify ing those fi ve nodes in the tree that are less well both Amphispiza and Ammodramus as polyphy- supported. Therefore, we consider Figure 2 our letic genera, corroborating the results of Carson most reliable estimate of these relationships and Spicer (2003). One of the strengths of this (a er Lanyon 1993). analysis is that it includes all likely members of this clade, enhancing the likelihood that the Discussion supported relationships shown refl ect the true species relationships. We discuss below, in Systematics overview.—We describe a well- greater detail, some of our salient fi ndings from defi ned clade that includes most of the elements a historical and taxonomic perspective. of the historical grassland sparrow assemblage Relationships within our Ammodramus but also all members of the genus Melospiza, one “phylogeny” are novel with respect to earlier 546 Klicka and Spellman [Auk, Vol. 124

Fig. 2. Consensus tree based on MP, ML, and Bayesian analyses with all weakly supported nodes collapsed. This tree represents our most “reliable estimate” (Lanyon 1993) of phylogenetic relationships among members of this clade. Subclades identified as (A) and (B) are discussed in the text.

taxonomies (Table 1; also see review in Murray sparrow clade is among our more striking fi nd- 1968), though some of the relationships we ings, though similar results were obtained by uncovered are refl ected in those eff orts. For Carson and Spicer (2003). The taxonomy of the example, the species leconteii, caudacutus (nel- genus has long been centered around savanna- soni) (considered a subspecies of caudacutus rum, the type species for this genus (Swainson by most taxonomists at the time), maritimus, 1827). Our results with respect to the genus and henslowii were treated as a group, fi rst as Ammodramus are similar to those obtained by Ammodramus (Ridgway 1901), then as Ammospiza Zink and Avise (1990), who analyzed mtDNA (Oberholser 1905), and later as Passerherbulus restriction fragments and allozymes. They also (Stone 1907, AOU 1910). Our analyses indi- identifi ed a well-resolved caudacutus–(nelsoni)– cate that caudacutus, nelsoni, maritimus, and maritimus–leconteii clade and suggested that leconteii form a well-resolved clade (Fig. 2A). henslowii and bairdii represent a “relatively old Ammodramus henslowii was paired with bair- sister species pair.” Their work, however, was dii in all our analyses (but always with low hindered by incomplete taxon sampling. They support). Although henslowii and bairdii are recognized that savannarum, humeralis, and auri- typically placed near each other, linear tax- frons were “genetically distinct from the others” onomies had not previously suggested a sister and that the genus Ammodramus “is possibly not relationship, and none has suggested a closer monophyletic,” but they lacked the data neces- relationship with Passerculus (and Melospiza) sary to document correct generic limits. than with the other members of Ammodramus. Xenospiza baileyi, a Mexican highland endemic, That savannarum, humeralis, and aurifrons are occurs today only in sacaton bunch grass not members of the reconfi gured grassland (Sporobolus sp.) habitat in La Cima Pass between April 2007] Grassland Sparrow Systematics 547

Mexico City and Cuernavaca. Specimen records ecological affi liations traditionally used to defi ne from a disjunct population in the Sierra de Bolaños sparrow assemblages are of questionable taxo- region of Jalisco exist, but the species was not nomic utility (see below). These results also (once found there in recent surveys (J. Klicka unpubl. again) emphasize that hybridization events can data). The correct placement of this sparrow has be a poor measure of phylogenetic relatedness long been a topic of a taxonomic controversy, (Prager and Wilson 1975, Klicka et al. 2001). which continues to this day. Xenospiza evidently The newly defi ned grassland sparrow clade possesses a suite of morphological characters includes three additional taxa, Pooecetes gramin- that suggest a variety of diff erent generic-level eus, Oriturus supercilisosus, and Amphispiza belli, assignments. In describing this species, Bangs of which the fi rst two represent monotypic gen- (1931) emphasized color and plumage pa erns era. These three are morphologically disparate and placed it among the grassland sparrows, taxa, bearing li le resemblance to one another believing that it was most similar to Ammodramus or to other members of this clade. Oriturus is leconteii. Pitelka (1947) dismissed these characters a large, bulky sparrow that is endemic to the as “superfi cial” and concluded that in characters highlands of northwestern and central Mexico, of size, proportions, and wing and tail shape, where it occupies bunch grasses and open pine Xenospiza was most similar to Melospiza lincolnii woods. In form, Oriturus resembles some mem- of the brushland sparrow group. Believing that bers of the genus Aimophila. Pooecetes breeds data on nests, eggs, juvenal plumages, song, and widely across middle and northern latitudes behavior provide “a more reliable basis for evalu- of North America, in open habitats including ating the systematic relationship of this elusive grasslands, shrubsteppe, and fallow croplands. sparrow,” Dickerman et al. (1967) considered it It is a medium-sized, rather typical “streaky- closest to other “grassland-nesting” sparrows, brown” sparrow that also possesses a unique though these authors suggested that without combination of morphological characters more compelling evidence it should be retained including a white eye ring, white outer rectri- as a monotypic genus. Each of these authors was ces, and a chestnut-colored scapular patch. We partly correct. According to our results, Xenospiza suggest that both these species remain mono- is embedded within the grassland sparrow clade, typic only because diagnostic morphological within which it is placed as sister to the three clues to relationships are lacking. The genus members of the traditional brushland sparrow Amphispiza comprises three species, accord- genus, Melospiza. The remaining members of the ing to some authors (e.g., Sibley and Monroe putative brushland sparrow complex, Zonotrichia, 1990): belli, bilineata, and quinquestriata. Others Junco, and Passerella, are elements of a well- have merged one (quinquestriata; Paynter and resolved clade (J. Klicka unpubl. data) that lies Storer 1970, AOU 1998) or all (Phillips et al. outside of the grassland clade and its sister, from 1964, Mayr and Short 1970) of these species into which outgroups were chosen. Aimophila. Our results confi rm polyphyly for The “brush-inhabiting” (Paynter 1964) or this genus (Carson and Spicer 2003), because “brushland-nesting” sparrows (Dickerman et belli is without question a member of the clade al. 1967) (Passerella, Melospiza, Zonotrichia, and of focus. Amphispiza quinquestriata does not Junco) have long been considered closely allied belong among the Aimophila (contra Paynter and species. This was a ributable, at least in part, Storer 1970, AOU 1998, Pa en and Fugate 1998), to a number of well-documented intergeneric but is instead sister to bilineata and closest to hybridizations (e.g., Dickerman 1961, Short and Chondestes and Calamospiza (J. Klicka unpubl. Simon 1965). Largely for this reason, Passerella, data; see Carson and Spicer 2003). Melospiza, and Zonotrichia have previously been Utility of morphological characters.—The com- lumped into the genus Zonotrichia (Paynter position of our “grassland” sparrow clade, and 1964); Short and Simon (1965) went a step fur- the relationships among its component taxa, ther, lumping all four of these genera into Junco. diff er from all previous morphology-based Within this assemblage, Melospiza and Passerella taxonomic hypotheses. That is, morphological are most similar morphologically, which leads and genetic estimates of relationships for this some authors to merge the two (e.g., Linsdale group are incongruent. Generic-level relation- 1928, Mayr and Short 1970). Our results suggest ships among sparrows have been the focus of that many of the morphological characters and a single modern, phylogenetic study (Pa en 548 Klicka and Spellman [Auk, Vol. 124 and Fugate 1998) using the structural and whose members share suites of morphological plumage characters used traditionally by avian characters. We do not doubt that some tradi- taxonomists. Not surprisingly, the results of tional taxonomic characters may be phyloge- that study supported the monophyly of all cur- netically informative. The challenge before us rently accepted genera. In that work, species of is to identify those characters that are reliable Ammodramus sampled included henslowii, bair- indicators of relationships and those homoplas- dii, and savannarum. Our study indicates that tic characters that are not. the taxonomic affi nities of the la er lie well out- Utility of ecological characters.—Robins and side this clade. Pa en and Fugate’s (1998) analy- Schnell (1971) performed a thorough phenetic sis also recovered other traditional groupings, analysis of the grassland sparrow complex, mea- such as the linking of Melospiza with Passerella, suring 48 skeletal features of multiple exemplars and Amphispiza belli with A. bilineata; both are for each putative member of the group. They incorrect, according to the molecular evidence. concluded that the assemblage should be divided It is diffi cult to fault earlier eff orts that were into two genera. Their clade of Ammodramus unable to recover our phylogeny. The compo- comprised savannarum, humeralis (aurifrons), bair- nent species of our grassland sparrow clade are dii, and P. sandwichensis, whereas their clade of a morphologically heterogeneous assemblage, Ammospiza contained leconteii, caudacuta (nelsoni), and we know of no nonmolecular taxonomic maritimus, henslowii, and X. baileyi. These authors characters that would suggest that they form noted that all species of the la er “breed in or a group. Furthermore, from the perspective of near marshes” and gave them the name “marsh- traditional taxonomy, it is diffi cult to examine land sparrows.” Similarly, because of habitat specimens and not come away with the impres- association, members of their Ammodramus clade sion that A. savannarum belongs somewhere were designated the “grassland” sparrows. It is near the other Ammodramus taxa and that well known that trees derived from morphologi- Melospiza and Passerella are most similar to one cal comparisons can refl ect a history of adaptive another. Traditional comparative methods sup- responses, which may or may not coincide with port these relationships. At some taxonomic phylogenetic history (Endler 1982). Results of levels and for some groups, morphological the present study and those of Zink and Avise cues indeed provide adequate representation (1990) indicate that the morphometric analyses of taxon relationships. For example, both mor- of Robins and Schnell (1971) identifi ed eco- phological and molecular characters identify a logical associations rather than true evolution- clade of Melospiza spp. and a group of “sharp- ary relationships. For clarity, we have used the tailed” Ammodramus species (Fig. 2A). By terms “grassland” and “brushland” to describe contrast, however, the traditional placement putative ecological and evolutionary sparrow of the savannarum–humeralis–aurifrons assem- assemblages. The original confi gurations of both blage within the grassland sparrow group these groups are polyphyletic, which suggests likely represents a case of morphological con- that generalized and simplistic ecological asso- vergence, a potential pitfall for morphological ciations may have limited value for phylogenetic analyses. Rather abrupt shi s in morphology inference. The single sparrow clade of study can also lead to incorrectly defi ned relation- contains “grassland” and “brushland” forms but ships, particularly among genera. For example, also species that are restricted to montane, low- the genus Melospiza had not previously been land, mesic, or xeric environments. With respect recognized as a member of this clade, despite to habitat preference, this is a heterogeneous the fact that it appears to be embedded within group, and among-lineage habitat shi s occur it. Morphologically, Melospiza departs from regularly within the sparrows studied. an otherwise uniform “Bauplan” that links Taxonomic implications.—Because our study the members of Ammodramus and Passerculus. benefi ts from thorough taxonomic sampling Also problematic for morphological taxonomy and identifi es several well-resolved nodes, we are those taxa with no close relatives. In our believe that the following suggested nomen- clade, Oriturus, Pooecetes, and Amphispiza belli clatural changes are justifi ed. The polyphyly of represent relatively basal lineages with no sub- Ammodramus necessitates either the naming of sequent bifurcations. These “older” species are new genera or the resurrection of former generic diffi cult to place within the context of genera designations. The type species for this genus April 2007] Grassland Sparrow Systematics 549 is savannarum (A. bimaculatus; Swainson 1827). and D. Nicolson kindly provided advice on This generic epithet must therefore remain nomenclatural changes. We thank C. Cicero and with the savannarum–humeralis–aurifrons clade two additional reviewers for their constructive that lies outside of our clade of interest. We comments on an earlier dra of this manu- suggest that the genus Ammospiza (Oberholser script. This work was funded, in part, by NSF 1905) be resurrected for the leconteii–caudacutus– DEB 0315469 (to J.K.) and the Barrick Museum nelsoni–maritimus clade (Fig. 2A). This name Foundation. has taxonomic priority and, with the addition of leconteii, reverts to the AOU (1957) check- Literature Cited list. The Xenopiza–Melospiza–Ammodramus (in part)–Passerculus clade (Fig. 2B) is a bit more Alfaro, M. E., S. Zoller, and F. Lutoni. 2003. problematic. Likely, some taxonomists would Bayes or bootstrap? A simulation study favor merging Xenospiza and Melospiza, resur- comparing the performance of Bayesian recting the genus Passerherbulus (Stone 1907) for Markov chain Monte Carlo sampling and henslowii and bairdii, and retaining Passerculus bootstrapping in assessing phylogenetic con- as a monotypic form. Such a taxonomy would fi dence. Molecular Biology and Evolution 20: be consistent with the relationships depicted 255–266. in Figure 1. However, Figure 2B indicates that American Ornithologists’ Union. 1886. The precise relationships within the group remain Code of Nomenclature and Check-list of North equivocal. A henslowii–bairdii sister relationship American Birds. American Ornithologists’ is not certain, nor is the relationship of this puta- Union, New York. tive pair with either Melospiza or Passerculus. To American Ornithologists’ Union. 1895. Check- accommodate this uncertainty and refl ect the list of North American Birds, 2nd ed. known evolutionary pa ern, we advocate merg- American Ornithologists’ Union, New York. ing all these taxa (Fig. 2B) into a single genus. American Ornithologists’ Union. 1910. Check- Among the genera listed, Passerculus (Bonaparte list of North American Birds, 3rd ed. American 1838) has priority and should be used. The long Ornithologists’ Union, New York. branches of Pooecetes, Amphispiza, and Oriturus American Ornithologists’ Union. 1957. Check- suggest a more distant relationship with other list of North American Birds, 5th ed. American clade members and an uncertain placement Ornithologists’ Union, Baltimore, Maryland. within the group. This uncertainty should be American Ornithologists’ Union. 1998. Check- refl ected by the retention of their monotypic list of North American Birds, 7th ed. American names. Thus, Pooecetes and Oriturus would Ornithologists’ Union, Washington, D.C. remain as they are; A. belli, however, presents a Bangs, O. 1931. A new genus and species of more diffi cult taxonomic problem. The type spe- American buntings. Proceedings of the New cies for the genus Amphispiza is bilineata (Coues England Zoological Club 12:85–88. 1874), which, along with A. quinquestriata, occurs Bonaparte, C. L. 1838. A Geographical and well outside our study clade. With that name Comparative List of Birds of Europe and taken, belli is alone at the generic level and in North America. John Van Voort, London. need of a generic epithet. Throughout much of Brandley, M. C., A. Schmit, and T. W. Reeder. its breeding range, this sparrow is associated 2005. Partitioned Bayesian analyses, with sagebrush (Artemesia tridentata) habitats, partition choice, and the phylogenetic and a descriptive name incorporating this asso- relationships of scincid lizards. Systematic ciation may be appropriate. 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