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Complex biogeographic history of a Holarctic passerine

Proceedings of the Royal Society B

April 2004
271(1538):545-51

DOI:10.1098/rspb.2003.2638

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PubMed

Authors:

Robert Zink

University of Nebraska at Lincoln

Sievert Rohwer

University of Washington Seattle

Igor Fadeev

State Darwin Museum

Show all 8 authorsHide

Our analysis of the ND2 sequences revealed six clades within winter wrens (Troglodytes troglodytes). These clades corresponded to six geographical regions: western Nearctic, eastern Nearctic, eastern Asia, Nepal, Caucasus and Europe, and differed by 3-8.8% of sequence divergence. Differences among regions explained 96% of the sequence variation in winter wren. Differences among individuals within localities explained 3% of the sequence variation, and differences among localities within regions explained 1%. Grouping sequences into subspecies instead of localities did not change these proportions. Proliferation of the six clades coincided with Early and Middle Pleistocene glaciations. The distribution of winter wren clades can be explained by a series of five consecutive vicariant events. Western Nearctic wrens diverged from the Holarctic ancestor 1.6 Myr before the present time (MYBP). Eastern Nearctic and Palaearctic wrens diverged 1 MYBP. Eastern and western Palaearctic birds diverged 0.83 MYBP. Nepalese and east Asian wrens diverged 0.67 MYBP, and Caucasian birds diverged from European wrens 0.54 MYBP. The winter wren has a much greater degree of inter- and intracontinental differentiation than the three other Holarctic birds studied to date--dunlin (Calidris alpina), common raven (Corvus corax) and three-toed woodpecker (Picoides trydactylus)--and represents an example of cryptic speciation that has been overlooked.

Geographical regions, localities, sample sizes and mismatch distributions. Vicariant events are labelled with the letter 'V' and their consecutive number. Mismatch distributions: x-axis, number of pairwise differences; y-axis, observations. Solid lines, observed distributions; dashed lines, expected distributions; vertical lines, mean mismatch. The p-values are for the differences from expectation of sudden population expansion.

…

Maximum-likelihood tree of unique haplotypes. Sample numbers are listed at the tips (for localities and subspecies see electronic Appendix A). Numbers next to branches indicate ML bootstrap values (100 replicates with random addition of taxa) and branch lengths (substitution/site).

…

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doi: 10.1098/rspb.2003.2638

, 545-551271 2004 Proc. R. Soc. Lond. B

Karagodin, Evgeniy A. Koblik and Yaroslav A. Red'kin

Sergei V. Drovetski, Robert M. Zink, Sievert Rohwer, Igor V. Fadeev, Evgeniy V. Nesterov, Igor

Complex biogeographic history of a Holarctic passerine

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on May 24, 2011rspb.royalsocietypublishing.orgDownloaded from

Received 26 September 2003

Accepted 4 November 2003

Published online 21 January 2004

Complex biogeographic history of a Holarctic

passerine

Sergei V. Drovetski

, Robert M. Zink

1,2

, Sievert Rohwer

, Igor V. Fadeev

Evgeniy V. Nesterov

, Igor Karagodin

†, Evgeniy A. Koblik

and Yaroslav A. Red’kin

Department of Ecology, Evolution and Behavior, and

Bell Museum, University of Minnesota, 100 Ecology Building,

1987 Upper Buford Circle, St Paul, MN 55108, USA

Burke Museum and Department of Zoology, University of Washington, Seattle, WA 98195-3010, USA

State Darwin Museum, 57 Vavilova Street, Moscow 117292, Russia

Zoological Museum, Moscow State University, Bol’shaya Nikitskaya Street 6, Moscow, 103009 Russia

Our analysis of the ND2 sequences revealed six clades within winter wrens (Troglodytes troglodytes). These

clades corresponded to six geographical regions: western Nearctic, eastern Nearctic, eastern Asia, Nepal,

Caucasus and Europe, and differed by 3–8.8% of sequence divergence. Differences among regions

explained 96% of the sequence variation in winter wren. Differences among individuals within localities

explained 3% of the sequence variation, and differences among localities within regions explained 1%.

Grouping sequences into subspecies instead of localities did not change these proportions. Proliferation

of the six clades coincided with Early and Middle Pleistocene glaciations. The distribution of winter wren

clades can be explained by a series of five consecutive vicariant events. Western Nearctic wrens diverged

from the Holarctic ancestor 1.6 Myr before the present time (MYBP). Eastern Nearctic and Palaearctic

wrens diverged 1 MYBP. Eastern and western Palaearctic birds diverged 0.83 MYBP. Nepalese and east

Asian wrens diverged 0.67 MYBP, and Caucasian birds diverged from European wrens 0.54 MYBP. The

winter wren has a much greater degree of inter- and intracontinental differentiation than the three other

Holarctic birds studied to date—dunlin (Calidris alpina), common raven (Corvus corax) and three-toed

woodpecker (Picoides trydactylus)—and represents an example of cryptic speciation that has been overlooked.

Keywords: winter wren; biogeography; phylogeography; speciation; vicariance; Holarctic

1. INTRODUCTION

Very little is known about the phylogeographic structure

of avian Holarctic species. Zink et al. (1995) surveyed 13

species inhabiting both Eurasia and North America and

found that 11 species showed at least some degree of intra-

specific differentiation in mitochondrial DNA (mtDNA)

between continents. Only three studies addressed large-

scale phylogeography of Holarctic avian taxa. Wenink et

al. (1996) found three distinct mitochondrial clades of

dunlin (Calidris alpina) corresponding to three large geo-

graphical regions: Europe, Canadian Arctic and

Siberia/Alaska. The latter was subdivided into three sub-

clades: west Siberian, east Siberian and Alaskan. The

Canadian clade was the most distantly related to the other

two clades and differed from them by 3.3% of uncorrected

sequence divergence of the most variable domains, I and

II of the mitochondrial control region (CRI and CRII;

Wenink et al. 1996). Omland et al. (2000) found no differ-

entiation in mtDNA between common ravens (Corvus

corax) from Eurasia and North America. However, birds

from western North America, south of the Canadian bor-

der, formed a distinct clade that was the sister to the Chi-

Author and address for correspondence: Department of Biological

Sciences, University of Alaska Anchorage, 3211 Providence Drive,

Anchorage, AK 99508, USA (svd@uaa.alaska.edu).

† Present address: Igor’s Taxidermy, 2931 S. Main Street, suite D, Santa

Ana, CA 92707, USA.

Proc. R. Soc. Lond. B (2004) 271, 545–551 545  2004 The Royal Society

DOI 10.1098/rspb.2003.2638

huahua raven (C. cryptoleucus), and was well differentiated

from the Holarctic raven (2.69% of uncorrected diver-

gence in the cytochrome b gene and 2.14% in CRI; calcu-

lated from Omland et al. (2000), Table 1). By contrast,

mtDNA of three-toed woodpeckers (Picoides tridactylus)

from Eurasia and North America differed by ca.4%

despite the lack of phylogenetic structure within conti-

nents (Zink et al. 2002). Both the common raven and the

three-toed woodpecker are uniformly distributed across

boreal regions of both continents.

Unlike the dunlin, which inhabits primarily arctic tun-

dra, but similar to the common raven and three-toed

woodpecker, the winter wren (Troglodytes troglodytes)is

widely distributed across the temperate zone of the Hol-

arctic. However, in both continents it is widely distributed

in a north–south direction only in the eastern and western

parts of the continents. In the middle of both continents,

its distribution has large gaps. In the Nearctic, the eastern

and western parts of the range are connected by a narrow

strip of habitat extending across Manitoba, Saskatchewan

and Alberta. In the Palaearctic, the eastern and western

parts of the range are separated by a narrow gap between

south-central and extreme eastern Turkmenistan

(Brewer 2001).

This distribution pattern and sedentary/limited

migration lifestyle of winter wren could result in genetic

differentiation at different scales, namely within and

between continents. The winter wren is one of the most

complex and phenotypically diverse taxa. Brewer (2001)

on May 24, 2011rspb.royalsocietypublishing.orgDownloaded from

546 S. V. Drovetski and others Biogeography of a Holarctic passerine

listed 39 subspecies, and noted that many more were

described in the Nearctic. The majority of winter wren

subspecific designations are based on slight variations of

plumage coloration and intensity of underbody barring.

Some geographically proximate subspecies of winter wren

form groups that are distinguished by their appearance

and vocalization. In the Nearctic, there are three pheno-

typically distinct groups: eastern, western and

Alaska/Aleutian (Pyle 1997; National Geographic Society

1999). In the Palaearctic, eastern Asian winter wrens dif-

fer from European and western and central Asian birds by

much darker brown plumage (Stepanyan 2003). Interest-

ingly, birds from the western Nearctic and eastern Asia,

and birds from the eastern Nearctic and Europe, are more

similar in appearance to each other than to birds from

opposite sides of their respective continents.

The complex geographical pattern of phenotypic vari-

ation has fostered much confusion about the evolutionary

and biogeographic history of the winter wren. Although a

generally accepted hypothesis suggests that the Palaearctic

was colonized by the western Nearctic birds through the

Bering Strait (Brewer 2001), alternative hypotheses were

proposed by several authors. For example, Hejl et al.

(2002) suggested separate invasions of the Palaearctic by

both eastern and western Nearctic winter wrens (Hejl et

al. 2002). Interestingly, all of these hypotheses are based

on dispersal scenarios, and none considers vicariance.

Some authors argue that because any distribution pattern

can be explained by numerous, equally parsimonious dis-

persal hypotheses, vicariance should be ruled out first, and

dispersal should be invoked when vicariance fails to

explain observed distribution patterns (Ronquist 1997).

We present data on large-scale phylogeographic pat-

terns in the Holarctic winter wren, and compare popu-

lation genetics parameters among localities with relatively

large sample sizes. We also discuss the historical biogeog-

raphy of winter wren and use dispersal–vicariance analysis

(DIVA; Ronquist 1996, 1997) to determine if vicariance

alone is sufficient to explain the observed geographical

structuring of winter wren haplotypes.

2. MATERIAL AND METHODS

A total of 97 winter wren samples were obtained from 24

localities across the Holarctic (figure 1). We also used 16 indi-

viduals of 14 wren species as outgroups (electronic Appendix A;

available on The Royal Society’s Publications Web site).

Total genomic DNA was extracted from frozen or 96% etha-

nol-preserved tissue samples using a QIAamp Tissue Kit

(QIAGEN Inc.). Each individual complete mitochondrial ND2

gene (1041 bp) was amplified with Perkin-Elmer PCR reagents

and primers L5215 (Hackett 1996) and H1064 (CTTTGA

AGGCCTTCGGTTTA, designed by S.V.D.). The PCR frag-

ments were sequenced directly on an ABI-3700 sequencer.

Sequences were aligned automatically by Sequencher 3.1.1

(Gene Codes Corporation). The alignment did not require edit-

ing because there were no indels in the ND2 sequences. A

maximum-likelihood (ML) phylogenetic analysis was performed

using PAUP

∗

(Swofford 1998). ML model and parameters were

determined by the hierarchical likelihood ratio test (hLRT) in

Modeltest 3.06 (Posada & Crandall 1998). Taxa were added

Proc. R. Soc. Lond. B (2004)

randomly for both ML and its bootstrap analysis (100

replicates). Population genetics parameters were calculated in

Arlequin 2.000 (Schneider et al. 2000). DIVA (Ronquist 1996,

1997) with its default settings was used for reconstruction of the

biogeographic history of winter wren.

3. RESULTS

(a) Geographical structuring of winter wren

haplotypes

The initial phylogenetic analysis (results not shown)

indicated that winter wrens are most closely related to

marsh (Cistothorus palustris) and sedge (C. platensis) wrens

than to the other outgroup species (electronic Appendix

A), including two members of Troglodytes: northern house

wren (T. aedon) and mountain wren (T. solstitialis). There-

fore, we used marsh and sedge wrens as outgroups for the

phylogenetic analysis of winter wren haplotypes.

Among 97 individuals of winter wren, 51 unique haplo-

types were distinguished based on 126 variable sites (120

transitions and nine transversions). The hLRT selected

the TrN⫹G model (Posada & Crandall 1998) for com-

plete ND2 sequences of winter, marsh and sedge wrens.

The TrN⫹G is a submodel of the general time reversible

(GTR) model (Rodrı

guez et al. 1990) in which transver-

sions are weighted equally and the discrete-gamma model

of substitution rates across sites (Yang 1994) is included.

Guanine was under-represented and cytosine was

over-represented in ND2 sequences (A = 30.08%,

C = 39.62%, G = 10.26%, T = 20.04%; G-test p = 0.0110).

All taxa shared this nucleotide bias and there was no evi-

dence of heterogeneity of base composition among taxa.

GenBank accession numbers for ND2 sequences are

AY460221–AY460333.

The ML analysis of wren haplotypes resulted in a

single tree. The molecular clock assumption for this tree

was not rejected (⫺ln L without molecular clock

enforced = 3092.786 33, ⫺ln L with molecular clock

enforced = 3124.447 44; ⫺2⌬ln L = 63.322 22, d.f. = 51,

p = 0.1154). Winter wren haplotypes formed six geo-

graphically concordant clades (figure 2). These clades cor-

responded to six major geographical regions: Europe,

Caucasus, Nepal (central Asia), eastern Asia, eastern

Nearctic and western Nearctic (figure 1). Each clade was

supported by bootstrap values of greater than or equal to

78%. The relationships among these clades, however,

were not strongly supported except for the sister-group

relationship of Caucasian and European clades, which

received 94% bootstrap support (figure 2).

The Palaearctic clades were divided into two pairs of

sister clades: the east Asian clade and a single haplotype

from Nepal (3.7% ML divergence between clades exclud-

ing intraclade variation), and European and Caucasian

clades (3.0% ML divergence). The ML divergence

between these pairs was 4.6%. Palaearctic birds were more

closely related to the eastern Nearctic clade (5.6% ML

divergence) than to the western Nearctic clade (8.8% ML

divergence), so the two Nearctic clades were not sisters.

Conversion of the node depths (excluding intraclade vari-

ation; figure 2) into million years before the present time

(MYBP) using an ND2 molecular clock calibration for

on May 24, 2011rspb.royalsocietypublishing.orgDownloaded from

Biogeography of a Holarctic passerine S. V. Drovetski and others 547

eastern

Asia

Europe

Caucasus 10

western

Nearctic

Ontario 4

MN 9

MI 2

ME 1

eastern

Nearctic

Nepal

Buryatiya 1

Khabarovsk

Sakhalin

Honshu

Moscow 5

Greece 1

Germany

Attu

Adak

AK 2

WA16

NY 4

MA 1

NJ 1

St Paul

Switzerland

Minnesota

p = 0.275

Honshu

p = 0.030

Caucasus

p = 0.404

Washington

p = 0.245

0123

12345 6

1234

1234567

Figure 1. Geographical regions, localities, sample sizes and mismatch distributions. Vicariant events are labelled with the letter

‘V’ and their consecutive number. Mismatch distributions: x-axis, number of pairwise differences; y-axis, observations. Solid

lines, observed distributions; dashed lines, expected distributions; vertical lines, mean mismatch. The p-values are for the

differences from expectation of sudden population expansion.

Galapagos mocking birds (0.0276 substitutions per site

per lineage Myr

⫺1

; B. S. Arbogast, P. T. Boag, G. Seutin,

P. R. Grant, B. R. Grant, S. V. Drovetski, R. Curry and

D. J. Anderson, unpublished data) indicated that winter

wrens radiated into the six lineages in Early–Middle Pleis-

tocene. The western Nearctic clade diverged from the

common ancestor of the other winter wren clades first, ca.

1.6 MYBP. The eastern Nearctic birds diverged from the

common ancestor of the Palaearctic clades ca. 1 MYBP.

Proc. R. Soc. Lond. B (2004)

Eastern and western Palaearctic winter wrens diverged

0.83 MYBP. East Asian birds and Himalayan birds

diverged 0.67 MYBP, and Caucasian and European birds

diverged last, 0.54 MYBP. Although sedge and marsh

wrens may not be the closest relatives of the winter wren,

divergence between the common ancestors of these two

lineages occurred 13 MYBP. Therefore, winter wren

could have existed since the Middle Miocene, long before

the radiation of the six current clades.

on May 24, 2011rspb.royalsocietypublishing.orgDownloaded from

548 S. V. Drovetski and others Biogeography of a Holarctic passerine

iuk263, svd1703, 1945, 2005

svd1999

svd2111

svd1774

svd1957

svd1966

svd1775

t437

svd2659, pac573

jk95019

svd2630

svd2850

grg3764

grg3765

grg3767

svd2383

evl295, sar7443, t1241, svd2382, 2844,

2848, grg3763, prs309,

1b2816-2819

svd2631, 2849

grg3766, prs235,

x7368

ksw2720, rwd24877

stp1

ksw1388, t713, gfb3209, 3217, mgs65,

svd1241, 2195, wlk37

cds4171

evl79

wlk49

gav903

nam255

svd2196

csw6240

svd2389

gav305

plg56

0.0146

0.0279

0.0434

western

Nearctic

eastern

Nearctic

Caucasus

00. 51. 01.5

Cistothorus palustris (sar7250)

C. platensis (ksw694, sdw50)

gav225

vm217

vm218

tt6, 7

tt3, 10, 12-13, 17-18, vm248

tt1, 11

tt4, 15

tt16

ty175

bks1020

svd297

tt2

jgg1149

db99.471

db00.127

ansp5325

9/23/02, db02.63, db99.64, b13472, rya,

bey98-99, iuk114, vm395,

svd2628, x8237, 8248, 8251

0.1185

0.2521

0.3248

0.0164

0.0053

0.0047

0.0176

0.0194

0.0077

0.0153

Europe

Nepal

eastern

Asia

100

b8855

Myr

Figure 2. Maximum-likelihood tree of unique haplotypes. Sample numbers are listed at the tips (for localities and subspecies

see electronic Appendix A). Numbers next to branches indicate ML bootstrap values (100 replicates with random addition of

taxa) and branch lengths (substitution/site).

Using PAUP

∗

we calculated average ML pairwise dif-

ferences among haplotypes within clades and their stan-

dard deviations (± s.d.). They were 0.34 ± 0.16% for the

western Nearctic, 0.26 ± 0.11% for the eastern Nearctic,

0.30 ± 0.14% for eastern Asia, 0.20 ± 0.08% for Europe

and 0.27 ± 0.11% for Caucasus.

Analysis of molecular variance (AMOVA; Excoffier et

al. 1992) indicated that most of the sequence variation

was due to differences among the six geographical regions.

Differences among individuals within populations

accounted for 3% of the sequence variation, differences

among localities within regions accounted for 1% of the

sequence variation, and differences among geographical

regions accounted for 96% of the sequence variation.

Proc. R. Soc. Lond. B (2004)

Grouping of haplotypes by subspecies rather than by

localities did not change the AMOVA results.

(b) Population genetics and demography of the

winter wren

Only one of the 11 localities with a sample size of four

or more had a marginally significant Tajima’s D-value

(Tajima 1989) indicating that the selective neutrality

assumption is appropriate for the evolution of ND2

sequences of winter wren (table 1).

The ML nucleotide diversity varied from 0 to 0.0029

(table 1). All European populations had very low nucleo-

tide diversities. British wrens were more genetically

diverse than birds from continental Europe, where 10

on May 24, 2011rspb.royalsocietypublishing.orgDownloaded from

Biogeography of a Holarctic passerine S. V. Drovetski and others 549

Table 1. Tajima’s p-values, age, nucleotide diversity based on ML (ML

␲

) and on infinite site model (

␲

), and their standard

deviations (s.d.) for populations with n ⭓ 4.

Tajima’s

locality npage (MYBP) ML

␲

s.d.

␲

s.d.

WA 16 0.047 0.038 0.002 104 0.001 642 0.002 017 0.001 330

MN 9 0.248 0.032 0.001 771 0.000 885 0.001 708 0.001 233

NY 4 0.284 0.018 0.000 968 0.000 617 0.000 961 0.000 952

Ontario 4 1.000 0.000 0.000 000 0.000 000 0.000 000 0.000 000

NC 5 0.079 0.051 0.002 835 0.001 383 0.002 690 0.001 986

Sakhalin Is. 4 0.739 0.052 0.002 870 0.001 560 0.002 722 0.002 147

Japan 14 0.177 0.019 0.001 041 0.000 669 0.001 035 0.000 813

GB 6 0.089 0.024 0.001 308 0.000 968 0.001 281 0.001 059

Moscow 5 1.000 0.000 0.000 000 0.000 000 0.000 000 0.000 000

Switzerland 4 1.000 0.000 0.000 000 0.000 000 0.000 000 0.000 000

Caucasus 10 0.266 0.037 0.002 043 0.001 264 0.001 964 0.001 358

birds from Switzerland, Germany and the Moscow region

shared a single haplotype. An application of the ND2 mol-

ecular clock indicates that all localities, except the three

localities covered by ice sheets (Ontario, Moscow and

Switzerland), were colonized by winter wrens before or

during the Last Glacial Cold Stage 0.021–0.017 MYBP

(Adams 2002). The three glaciated localities had all indi-

viduals sharing the same haplotype (figure 2), indicating

a very recent colonization of these areas by winter wrens.

The nucleotide diversity based on infinite site model

(

␲

) was slightly lower than nucleotide diversity based on

ML corrected distances (ML

␲

). However, the values

were strongly correlated (Y = 1.733 × 10

⫺5

⫹ 0.950 × X;

d.f. = 10, r

= 1, p ⬍ 0.0001).

Mismatch distributions were calculated for four

localities that had a sample size of nine or more (Japan,

Caucasus, Minnesota and Washington; figure 1). All four

localities were at similar latitudes 43°–48° N. Mismatch

distributions for Caucasus, Minnesota and Washington

had similar mean mismatch values and did not differ sig-

nificantly from the expectation of recent demographic

expansion (Slatkin & Hudson 1991; Rogers & Harpending

1992). By contrast, the mismatch distribution for the

Honshu sample differed significantly from that expected,

despite its apparent unimodality and its mean mismatch

value, which was half of each of the other three sample

values.

relationships

DIVA (Ronquist 1996, 1997) indicated that vicariance

alone is sufficient to explain the current distribution of

winter wren clades, and no dispersal has to be invoked.

According to DIVA reconstruction, the ancestral popu-

lation of winter wrens was widespread across the Holarc-

tic. The first divergence resulted from western Nearctic

birds separating from the Holarctic ancestor, presumably

because they were isolated in a southern area of western

North America at a time when Holarctic populations of

wrens were still exchanging genes across Beringia (figure

1). Consistent with this reconstruction of their early his-

tory is the fact that the songs of European, Japanese and

eastern North American wrens are much more similar to

each other than any of them is to the songs of winter wrens

from Washington and Oregon (Kroodsma & Momose

Proc. R. Soc. Lond. B (2004)

1991). This first divergence was followed by the separ-

ation of eastern Nearctic and Palaearctic birds. This

second split is likely to have involved isolation across

Beringia because prior to major Middle Pleistocene glaci-

ations, eastern Nearctic wrens could have occupied an

even larger portion of the northern Nearctic than they do

to date. Within the Palaearctic, the first divergence was

between the wrens of eastern and western Eurasia. Eastern

Palaearctic birds diverged into east Asian and central

Asian (represented by a single individual from Nepal in

our study) clades, and western Palaearctic birds diverged

into Caucasian and European clades (figure 1).

4. DISCUSSION

Our analysis identified six mtDNA clades of winter

wren. This differentiation was geographically structured

and clades corresponded to large geographical regions:

eastern Asia, Nepal (central Asia), Caucasus, Europe,

eastern Nearctic and western Nearctic. The differentiation

among the six clades was 3.0–8.8% of ML nucleotide

divergence. These deep divergences argue for recognition

of the six clades as evolutionarily significant units (Moritz

1994), or even species. Strong differentiation of winter

wren clades and the relationships among them are also

supported by differences in their vocalization

(Kroodsma & Momose 1991).

Virtually all sequence variation in winter wren was

explained by differences among the six regions (96%).

Differences among localities or subspecies within the six

regions explained only 1% of sequence variation. Subspe-

cies were not reciprocally monophyletic and many shared

haplotypes. Thus, subspecific divisions in winter wren do

not reflect the species’ evolutionary history, as found for

many other birds (Zink 2004). Unlike in most other cases,

however, the numerous subspecific divisions in winter

wren have obscured the recognition of deep, species-level,

evolutionary divisions.

Although an ancestral form could have existed since the

Middle Miocene (13 MYBP), proliferation of winter wren

into the six clades coincided with the Early and Middle

Pleistocene glaciations. Late Pleistocene glaciations did

not produce distinct clades, but presumably contributed

to self-pruning of the ND2 haplotype tree. In the localities

that were free of ice during the last glaciation, population

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550 S. V. Drovetski and others Biogeography of a Holarctic passerine

age does not exceed 52 000 years (middle of the previous

interstadial), which is an order of magnitude younger than

the age of the most recent divergence among the clades

(540 000 years).

Mismatch distributions (figure 1) suggested recently

expanding populations, except for the Honshu population,

whose mismatch distribution was significantly different

from that expected for a recently expanding population

despite its unimodal shape and low mean. Northward

expansion during the current interstadial could have

resulted in fragmentation of the southern parts of the spec-

ies’ range and in a loss of genetic variability in Japan

(Hewitt 2000). A recent loss of genetic variability can pro-

duce a unimodal mismatch distribution similar to that of

rapidly expanded populations. The slope of the distri-

bution plot in declining populations, however, is steeper,

especially on the right side of the graph, than in recently

expanded populations (Rogers & Harpending 1992).

Although the Japanese winter wren population appears

stable, our samples are from central Honshu, where wrens

are on the periphery of the core population to the north,

and where they have low breeding success (K. Ueda, per-

sonal communication). The loss of genetic variability in

Japanese winter wren is also supported by the fact that the

population from Daito Islands (800 km south of Kyushu)

recently became extinct and the population from Izu

Islands (just southeast of Honshu) is endangered

(Ministry of the Environment of Japan 1998). Further-

more, nucleotide diversity in Sakhalin Island, to the north

of Hokkaido, is 2.8 times greater than in central Honshu.

Declines in Japanese populations of some other temperate

species are also known. For example, in the 1970s Asian

rosy-finch (Leucosticte arctoa) probably bred in Hokkaido,

where adults and fledglings were observed during the

breeding season, but it no longer appears to breed in Japan

(Brazil 1991).

The current distribution of winter wren clades can be

explained by a sequence of five vicariant events (figure 1)

that were probably caused by Early and Middle Pleisto-

cene glaciations. These glaciations began periodic separ-

ations between the Nearctic and Palaearctic across

Beringia, and between regions within these continents.

Winter wrens could have had over 10 Myr to acquire a

wide Holarctic distribution during the Late Miocene and

Pliocene when the continents were connected across

Beringia and many animals dispersed from one continent

to the other. It is difficult to reconstruct the routes by

which winter wren may have spread throughout the Hol-

arctic because habitat distributions have changed dramati-

cally since the Miocene. For example, mountain ranges

currently inhabited by some clades (e.g. Caucasus,

Himalayas) developed during the Miocene. However,

colonization routes probably had little effect on differen-

tiation of the six clades because these clades seem to have

differentiated from a single, undifferentiated Holarctic

ancestor.

While the six clades discovered with our samples can

readily be explained by vicariance, dispersal may still be

needed to explain some aspects of the distribution of win-

ter wrens. Most obvious are the populations of winter

wrens currently inhabiting Iceland and other islands of the

North Atlantic. These islands could have been colonized

by dispersal from either Europe or the eastern Nearctic.

Proc. R. Soc. Lond. B (2004)

Samples from these islands, together with larger samples

from eastern North America and Europe, will be needed

to determine the source populations for these coloniza-

tions.

The winter wren appears to differ considerably in phylo-

geographic structure from the other three Holarctic avian

taxa studied to date. It is strongly differentiated within and

between continents and differences among clades are

much greater (almost threefold) than in the dunlin

(Wenink et al. 1996), the common raven (Omland et al.

2000) and the three-toed woodpecker (Zink et al. 2002).

Additional detailed population genetics studies of widely

distributed Holarctic taxa are needed to elucidate whether

these differences among taxa in the degree of intrataxon

differentiation are related to their ecology and dispersal

ability or to their demographic history.

Garrett Eddy sponsored all of the Burke Museum expeditions

to Russia in 1992–2000. D. A. Banin, V. B. Masterov, A. V.

Andreev and many other Russian colleagues provided help

with the logistics of the expeditions. Paul Kester helped with

references on palaeoecology. The majority of tissue samples

for this study came from the University of Washington Burke

Museum, with additional samples supplied by Dr Keisuke

Ueda, Rikkyo University, the University of Minnesota Bell

Museum, the British Natural History Museum, the University

of Michigan Museum of Zoology, the US National Museum

of Natural History, the Royal Ontario Museum, the University

of Alaska Museum, the Louisiana State University Museum

of Natural History, the Moscow State University Zoological

Museum, the American Museum of Natural History, and the

Academy of Natural Sciences of Philadelphia. S.V.D. was sup-

ported by a postdoctoral fellowship from the Department of

Ecology, Evolution and Behavior, University of Minnesota.

Molecular work for this project was funded by Garrett Eddy,

an EEB postdoctoral fellowship to S.V.D., and an NSF grant

DEB 9707496 to R.M.Z. and S.A.R. We are grateful to D.

Parkin and an anonymous reviewer for useful comments on

our manuscript.

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Varia: St Kilda Wren

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Article

Full-text available

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Article

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We compared mitochondrial DNA sequences of Three-toed Woodpeckers (Picoides tridactylus) within and between Eurasia and North America. Samples from the two continents are each reciprocally monophyletic, and differ by approximately 4% sequence divergence, suggesting that a separate species exists on each continent. We recommend formal taxonomic action. Within continents, no phylogeographic structuring was found, suggesting that both species have recently expanded their ranges following the end of the last ice age. Filogeografía Holártica y Límites de la Especie Picoides tridactylus Resumen. Comparamos secuencias de ADN mitocondrial en Picoides tridactylus, dentro y entre Eurasia y América del Norte. Las muestras de cada uno de los dos continentes son recíprocamente monofiléticas y difieren aproximadamente en un 4% de divergencia secuencial, sugiriendo que existe una especie distinta en cada continente. Recomendamos acción taxonómica formal. No encontramos estructura filogeográfica dentro de los continentes, sugiriendo que ambas especies han expandido recientemente sus rangos luego del final de la última era glacial.

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Global mitochondrial DNA phylogeography of holarctic breeding dunlins, Calidris alpina.

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Feb 1996
EVOLUTION

Comparison of mitochondrial DNA (mtDNA) control-region sequences of 155 dunlins from 15 breeding populations confirmed the existence of five major phylogeographic groups in the circumpolar breeding range of this migratory shorebird species. Time estimates of the origin of groups, based on sequence divergences and a molecular clock for birds, suggest a scenario of repeated fragmentation of populations in isolated tundra refugia during the late Pleistocene. The distribution of about three-quarters of all detected molecular variance between phylogeographic groups attests to the strongly subdivided genetic population structure in dunlins that is being maintained by natal philopatry. Each mtDNA phylogeographic group can be related to a morphometrically defined subspecies, but several other recognized subspecies are not supported by monophyletic mtDNA lineages within their purported ranges. More detailed analysis of several European populations reveals low amounts of gene flow and the partitioning of a substantial fraction of molecular variance between them. This ongoing evolution of population-genetic structuring within the European phylogeographic group most likely started with the last retreat of the ice sheets some 10,000 years ago. Dunlins thus provide one of the clearest examples of the linkage between historical and contemporary components of mtDNA phylogeographic structuring in birds.

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Article

May 1992

Episodes of population growth and decline leave characteristic signatures in the distribution of nucleotide (or restriction) site differences between pairs of individuals. These signatures appear in histograms showing the relative frequencies of pairs of individuals who differ by i sites, where i = 0, 1, .... In this distribution an episode of growth generates a wave that travels to the right, traversing 1 unit of the horizontal axis in each 1/2u generations, where u is the mutation rate. The smaller the initial population, the steeper will be the leading face of the wave. The larger the increase in population size, the smaller will be the distribution's vertical intercept. The implications of continued exponential growth are indistinguishable from those of a sudden burst of population growth Bottlenecks in population size also generate waves similar to those produced by a sudden expansion, but with elevated uppertail probabilities. Reductions in population size initially generate L-shaped distributions with high probability of identity, but these converge rapidly to a new equilibrium. In equilibrium populations the theoretical curves are free of waves. However, computer simulations of such populations generate empirical distributions with many peaks and little resemblance to the theory. On the other hand, agreement is better in the transient (nonequilibrium) case, where simulated empirical distributions typically exhibit waves very similar to those predicted by theory. Thus, waves in empirical distributions may be rich in information about the history of population dynamics.

PAUP*. Phylogenetic Analysis Using Parsimony (*and Other Methods). Version 4.0b10

Book

Jan 2002

David L. Swofford

— We studied sequence variation in 16S rDNA in 204 individuals from 37 populations of the land snail Candidula unifasciata (Poiret 1801) across the core species range in France, Switzerland, and Germany. Phylogeographic, nested clade, and coalescence analyses were used to elucidate the species evolutionary history. The study revealed the presence of two major evolutionary lineages that evolved in separate refuges in southeast France as result of previous fragmentation during the Pleistocene. Applying a recent extension of the nested clade analysis (Templeton 2001), we inferred that range expansions along river valleys in independent corridors to the north led eventually to a secondary contact zone of the major clades around the Geneva Basin. There is evidence supporting the idea that the formation of the secondary contact zone and the colonization of Germany might be postglacial events. The phylogeographic history inferred for C. unifasciata differs from general biogeographic patterns of postglacial colonization previously identified for other taxa, and it might represent a common model for species with restricted dispersal.

Songs of the Japanese Population of the Winter Wren (Troglodytes troglodytes)

Article

May 1991

An evaluation of the singing behavior of the Japanese wren (Troglodytes trog-lodytes fumigatus) might help to identify the origin of Old World wren populations and the forces that have molded the remarkable songs of this species throughout the Holarctic. The Japanese wrens seem identical to European wrens: males have repertoires of 6-7 highly repeatable song types of comparable duration and complexity. Wrens of eastern North America have a similar song organization, but the internal microstructure of songs is simpler and repertoires are only l-3 song types apiece. Both of these song populations are highly different from the wrens of western North America, which use songs with greater internal variety, more variable sequences of songs, and hence much larger repertoires of song types. These behavioral data are consistent with a hypothesis that populations in the mountainous regions of western North America were isolated before the "eastern" North American wren colonized the Old World, nrobablv via the Bering Straits. Not knowing the malleabilitv of these vocal behaviors under different life histories, however, makes such a phyletic con&u-sion highly tentative.

Dispersal-Vicariance Analysis: A New Approach to the Quantification of Historical Biogeography

Article

Nov 1996

Fredrik Ronquist

Quantification in historical biogeography has usually been based on the search for a single branching relationship among areas of endemism. Unlike organisms, however, areas rarely have a unique hierarchical history. Dispersal barriers appear and disappear and may have different effects on different species. As a result, the biota of an area may consist of several components with separate histories, each of which may be reticulate rather than branching. In an attempt to address these problems, I present a new biogeographic method, dispersal-vicariance analysis, which reconstructs the ancestral distributions in a given phylogeny without any prior assumptions about the form of area relationships. A three-dimensional step matrix based on a simple biogeographic model is used in the reconstruction. Speciation is assumed to subdivide the ranges of widespread species into vicariant components; the optimal ancestral distributions are those that minimize the number of implied dispersal and extinction events. Exact algorithms that find the optimal reconstruction(s) are described. In addition to their use in taxon biogeography, the inferred distribution histories of individual groups serve as a basis for the study of general patterns in historical biogeography, particularly if the relative age of the nodes in the source cladograms is known.

ARLEQUIN: A software for population genetics data analysis

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