University of Groningen From pampa to puna van Els, Paul ... fileJ Zool Syst Evol Res. 2019;57:485–496. wileyonlinelibrary.com/journal/jzs | 485 1 | INTRODUCTION The study of diversification

University of Groningen

From pampa to punavan Els Paul Norambuena Heraldo V Etienne Rampal S

Published inJournal of zoological systematics and evolutionary research

DOI101111jzs12278

IMPORTANT NOTE You are advised to consult the publishers version (publishers PDF) if you wish to cite fromit Please check the document version below

Document VersionPublishers PDF also known as Version of record

Publication date2019

Link to publication in University of GroningenUMCG research database

Citation for published version (APA)van Els P Norambuena H V amp Etienne R S (2019) From pampa to puna Biogeography anddiversification of a group of Neotropical obligate grassland birds (Anthus Motacillidae) Journal ofzoological systematics and evolutionary research 57(3) 485-496 httpsdoiorg101111jzs12278

CopyrightOther than for strictly personal use it is not permitted to download or to forwarddistribute the text or part of it without the consent of theauthor(s) andor copyright holder(s) unless the work is under an open content license (like Creative Commons)

Take-down policyIf you believe that this document breaches copyright please contact us providing details and we will remove access to the work immediatelyand investigate your claim

Downloaded from the University of GroningenUMCG research database (Pure) httpwwwrugnlresearchportal For technical reasons thenumber of authors shown on this cover page is limited to 10 maximum

Download date 16-01-2020

J Zool Syst Evol Res 201957485ndash496 wileyonlinelibrarycomjournaljzsemsp|emsp485

1emsp |emspINTRODUC TION

The study of diversification in Neotropical birds has been centered largely on the rich Amazonian and Andean forest biota as evidenced by an abundance of recent phylogenetic and phylogeographic stud-ies (eg Cuervo 2013 Fernandes Cohn- Haft Hrbek amp Farias 2015 Fjeldsaring Bowie amp Rahbek 2012 Harvey amp Brumfield 2015 Smith

et al 2014) Although forests have provided fruitful foci of study approximately 15 of South America is covered in various types of natural open lowland and montane grassland (Eva et al 2004) which hold a unique avifauna of open habitats The dynamics of diversifi-cation in open landscapes may differ greatly from those in forested habitats (Bates Tello amp Silva 2003) For example grassland taxa are presumably more vagile due to seasonal climatic fluctuations and

Accepted 7 February 2019

DOI 101111jzs12278

O R I G I N A L A R T I C L E

From pampa to puna Biogeography and diversification of a group of Neotropical obligate grassland birds (Anthus Motacillidae)

Paul van Els12 emsp| Heraldo V Norambuena34 emsp| Rampal S Etienne1

1Groningen Institute for Evolutionary Life Sciences University of Groningen Groningen The Netherlands2Department of Biological Sciences Museum of Natural Science Louisiana State University Baton Rouge LA3Departamento de Zoologiacutea Facultad de Ciencias Naturales y Oceanograacuteficas Universidad de Concepcioacuten Concepcioacuten Chile4Centro de Estudios Agrarios y Ambientales Valdivia Chile

CorrespondencePaul van Els Groningen Institute for Evolutionary Life Sciences University of Groningen Groningen The NetherlandsEmail paulvanelsgmailcom

AbstractThe evolution of Neotropical birds of open landscapes remains largely unstudied We investigate the diversification and biogeography of a group of Neotropical obligate grassland birds (Anthus Motacillidae) We use a multilocus phylogeny of 22 taxa of Anthus to test the hypothesis that these birds radiated contemporaneously with the development of grasslands in South America We employ the R package DDD to ana-lyze the dynamics of Anthus diversification across time in Neotropical grasslands explicitly testing for shifts in dynamics associated with the Miocene development of grasslands the putative Pleistocene expansion of arid lowland biomes and Pleistocene sundering of Andean highland grasslands A lineage- through- time plot revealed increases in the number of lineages and DDD detected shifts to a higher clade- level carrying capacity during the late Miocene indicating an early burst of di-versification associated with grassland colonization However we could not corrobo-rate the shift using power analysis probably reflecting the small number of tips in our tree We found evidence of a divergence at ~1 Mya between northern and southern Amazonian populations of Anthus lutescens countering Haffers idea of Pleistocene expansion of open biomes in the Amazon Basin We used BioGeoBears to investigate ancestral areas and directionality of colonization of Neotropical grasslands Members of the genus diversified into out of and within the Andes within- Andean diversifica-tion being mostly Pleistocene in origin

K E Y W O R D S

Andes dispersal Neotropical grasslands puna

This is an open access article under the terms of the Creative Commons Attribution-NonCommercial-NoDerivs License which permits use and distribution in any medium provided the original work is properly cited the use is non-commercial and no modifications or adaptations are madecopy 2019 The Authors Journal of Zoological Systematics and Evolutionary Research Published by Blackwell Verlag GmbH

Contributing authors Heraldo V Norambuena (buteonisgmailcom) Rampal S Etienne (rsetiennerugnl)

486emsp |emsp emspensp van ELS Et aL

fire regimes that force movements of grassland inhabitants (Hovick Elmore amp Fuhlendorf 2014 Little Hockey amp Jansen 2013) The abil-ity to disperse across the landscape is a major factor in determining rates of diversification in birds (Smith et al 2014) Increased disper-sal capacity may lead to increased gene flow among populations and a reduction in speciation but may also result in the establishment of new populations across landscape barriers and increased specia-tion rates through founder effects (ldquointermediate dispersal modelrdquo Claramunt Derryberry Remsen amp Brumfield 2012 Diamond Gilpin amp Mayr 1976 Phillimore Freckleton Orme amp Owens 2006)

The difference in geographic distribution of grasslands versus forest may also produce differences in the spatial patterns of diversi-fication in grassland versus forest birds Grasslands and other semi- arid habitats form a geographic complement to forests in much of South America In the Andes extensive grasslands occur almost ex-clusively between 2500 and 4800 m (Romaacuten- Cuesta et al 2014) Unlike Andean forests they represent the highest vegetation zone being often highly isolated from each other by intervening lower for-ested habitats that potentially act as barriers to gene flow (Cuervo 2013 Robbins amp Nyaacuteri 2014) In addition tropical grasslands are found in a ring around the Amazon Basin (ldquocircum- Amazonianrdquo dis-tribution Remsen Rocha Schmitt amp Schmitt 1991) with scattered pockets within the Amazon Basin The unique configuration of Neotropical grassland landscapes likely has a profound influence on the biogeography of grassland organisms and their phylogeography may differ considerably from those of better studied forest taxa

Grasslands also have very different origins from forests and this undoubtedly has had far- reaching consequences for the evolutionary trajectory of its inhabitants Similar to other continents the emergence of grasslands in the Neotropics occurred much later than the rise of forests (Pennington amp Hughes 2014) Whereas Neotropical grasslands originated during the Paleogene C3 cold- adapted grasslands were not widespread until the mid- Cenozoic and C4 warm- climate grasslands expanded much later during the late Neogene (Stroumlmberg 2011) There is some evidence that grassland- inhabiting organisms show an uptick in diversification during the development of grasslands (Agarwal amp Ramakrishnan 2017 Estep et al 2014 Neiswenter amp Riddle 2010) mainly during the Miocene Temporal estimates of the evolution of trop-ical C4 grasslands range from the early (Edwards Osborne Stroumlmberg amp Smith 2010 Stroumlmberg 2011) to late Miocene specifically for South America (Latrubesse et al 2010) If the Miocene spread of grasslands plays a role in the diversification of grassland- restricted organisms di-versification should on the contrary be fastest during or right after the Miocene when newly available grasslands were colonized

Many bird groups are too young to be used as a testing frame-work for a correlation between the Miocene spread of grasslands and diversification having diversified mainly during the Pliocene and Pleistocene under the influence of climatic fluctuations especially in temperate and montane areas (Lovette 2005 Weir 2006) The influence of Pleistocene climatic oscillations may be visible in the ge-netic makeup of organisms inhabiting high- elevation Andean grass-lands Although now often contested (Arruda Schaefer Fonseca Solar amp Fernandes- Filho 2017 Burkart 1975 Bush amp Oliveira

2006 Colinvaux 1998 Patel Weckstein Pataneacute Bates amp Aleixo 2011) Haffer (1969) postulated that the distribution of Neotropical lowland taxa was also strongly affected by Pleistocene climate changes Amazonian forest retreated to refugia whereas open drier habitats including grasslands dominated the Amazon Basin If this holds true the period during the height of the last glacial maximum that is characterized by a relatively large extent of dry biome should have left a distinct genetic footprint of shallow divergence or pan-mixia in Neotropical grassland organisms However these ideas have not been explicitly evaluated due to the lack of available information about the diversification of organisms of the Neotropical arid biome

To address this issue we focused on the diversification of a group of Neotropical grassland birds the Neotropical pipits (Anthus) which are represented in the New World by eleven species (South American Checklist Committee Remsen et al 2018) five of which are poly-typic All resident New World Anthus except for the North American A rubescens Tunstall 1771 and A cervinus Pallas 1811 form a mono-phyletic group (Pietersen Mckechnie Jansen Little amp Bastos 2018 Van Els amp Norambuena 2018 Voelker 1999ab) Neotropical pipits are obligate grassland birds and one of few grassland bird groups found in all temperate tropical and montane grassland areas in South America including some of the smaller Amazonian and Andean patches Hence this genus is ideal for exploring the timing rate geo-graphic direction and geographic variation of diversification of grass-land birds across Neotropical open landscapes

Some species of Anthus are known for regular (Mild amp Alstroumlm 2010) and irregular long- distance movements (Brinkhuizen Brinkhuizen Keaveney amp Jane 2010 Lees amp VanderWerf 2011 Voelker 2001) Voelker (1999b) assessed dispersal patterns at a broad mainly intercontinental scale within the entire genus using dispersal- vicariance analysis (DIVA) Methods have become avail-able that rely on likelihood calculation and incorporate several biologically relevant parameters (Matzke 2012) to investigate di-versification across the landscape These models can be combined with time- calibrated phylogenies to more accurately infer the timing and geography of dispersal patterns at a smaller intracontinental scale This will not only shed light on the direction of diversifica-tion in this group of grassland- dependent birds but also will allow us to further test the hypothesis that grassland bird diversification in South America is correlated with the spread of dry biomes on the continent In South America the genus Anthus is represented in lowland grasslands and the much younger climatically distinct but structurally similar montane grasslands In multiple cases Anthus species have populations at low and high elevations suggesting that the Andes may have been colonized from the lowlands However the directionality of these patterns is uncertain

In brief the aims of this study were (a) to test whether the timing and rates of diversification of Neotropical Anthus shifted with the Miocene spread of lowland grasslands in lowland taxa the putative Pleistocene expansion of Amazonian grasslands in tropical lowland taxa and the Pleistocene climatic oscillations in Andean taxa and (b) to resolve what was the geographic sequence of Anthuss spread to all major grassland areas on the South American continent across

emspensp emsp | emsp487van ELS Et aL

time to test the idea that the Andes were colonized multiple times from lowland grasslands

2emsp |emspMATERIAL S AND METHODS

21emsp|emspSamples and data collection

We obtained 39 tissue samples of all 22 subspecies- level taxa (Table 1) within the ldquoNew World Anthus claderdquo (Pietersen et al 2018 Van Els amp Norambuena 2018 Voelker 1999a) the remain-ing New World taxa belong to a mostly Asian clade Most taxa are represented by gt1 individual from localities as widely dispersed as possible within their ranges (Figure 1) Based on existing phylog-enies of Anthus we chose A cinnamomeus Ruumlppell 1840 A gustavi Swinhoe 1863 A rubescens and A rufulus Vieillot 1818 as out-groups because they represented closely related clades (Alstroumlm et al 2015 Voelker 1999a) We extracted total genomic DNA from pectoral muscle using a Qiagen DNeasy tissue extraction kit (QIAGEN Valencia California) following manufacturers protocol In a few cases we used toe pad tissue for which we first washed toe pads three times with ddH2O extended incubation to 24 hr and added dithiothreitol (DTT) to the incubation stage extended the elution step to 1 hr and eluted twice to a total volume of 300 μl after which we vacufuged the total volume down to 150 μl

We amplified one mitochondrial gene (NADH dehydrogenase subunit 2mdashND2) and three nuclear genes intron 2 of the myoglobin gene MYO (Heslewood Elphinstone Tidemann amp Baverstock 1998) intron 5 of the beta- fibrinogen gene FIB5 and intron 9 of the sex- linked gene for aconitase ACOI9 (Kimball et al 2009) We used the primer sequences listed in Supporting Information Table S1 for am-plification of mitochondrial and nuclear genes and designed several internal primers specific for Anthus for amplification of ancient DNA using Geneious 81 (Kearse et al 2012) We performed polymerase chain reactions (PCR) in 125 μl reactions using the following proto-col denaturation at 94degC for 10 min 40 cycles of 94degC for 30 s vari-able annealing temperatures and 72degC for 2 min followed by 10 min elongation at 72 and 4degC soak We used the program Sequencher (Gene Codes Corporation Ann Arbor Michigan) for alignment To detect and interpret insertions and deletions in the nuclear DNA we used the program Indelligent (Dmitriev amp Rakitov 2008) We phased sequences in DnaSP using the algorithm provided by PHASE (Stephens amp Donnelly 2003) with an ambiguity cutoff of gt07 No alignment gaps were left after these procedures so that amplicon length was the same as primer length plus alignments We deposited sequences in GenBank (accession numbers listed in Table 1)

22emsp|emspPhylogenetic analyses

We identified the best- fit nucleotide substitution model for each locus using jModeltest 2 (Darriba Taboada Doallo amp Posada 2012 Guindon amp Gascuel 2003) The HKY+I model was the best fit for all loci We recovered a species tree in BEAST a component of BEAST v 232 (Drummond amp Rambaut 2007) achieving ESS values gt200

for all parameter values We used a calibrated Yule prior and we ran the analysis for 100 million generations sampling every 1000 We analyzed posterior output in TRACER v 15 and specified a burn- in of 10 The mitochondrial ND2 locus was determined to evolve under a clocklike model in MEGA70 (Kumar Nei Dudley amp Tamura 2008 AIC = 2692016) We used a lognormal substitution rate prior with a mean of 29 times 10minus8 substitutionssiteyear (Lerner Meyer James Hofreiter amp Fleischer 2011) for ND2 and nuclear rates of 135 times 10minus9 substitutionssiteyear (Kimball et al 2009) applying lognormal distributions for most user- specified priors except for base- frequency proportions (uniform) and population size priors (Jeffreys) There are no fossil data from South America to describe the timing of diversification of the group but a fossil Anthus from Pliocene deposits (43ndash48 Mya) from southwestern Kansas shows features that overlap with mean morphometrics of A spraguei Audubon 1844 (Emslie 2007) and was used as a mini-mal age calibration point for this lineage as well as for the ancestor of Neotropical Anthus for a more conservative estimate

23emsp|emspDiversification analysis

To test for effects of diversity dependence across our tree we used the R package DDD v 35 (Etienne amp Haegeman 2012) which ena-bles maximum- likelihood estimations of diversity- dependent di-versification (function dd_ML) as well as testing for major shifts in these parameters across the tree (function dd_SR_ML ldquoshifting- rates modelrdquo) We explicitly tested for the effects of major climatic events on the dynamics of Anthus diversification by examining differ-ent models with fixed time parameters under a shifting- rate frame-work at 53 Mya (MiocenendashPliocene boundary to test for effects of C4 grassland spread in South America) at 40 Mya (start of forma-tion of uppermost Andean vegetation zones in older Central Andes Pennington amp Hughes 2014) at 20 Mya (end of formation of upper-most Andean vegetation zones in young northern Andes Pennington amp Hughes 2014) and at 18 Mya (start of Quaternary glaciations) We used a subset of the data excluding subspecies abariensis of A lutes-cens Pucheran 1855 because of its genetic closeness to subspecies parvus and using one lowland and one highland lineage as representa-tives of the poorly differentiated A correndera Vieillot 1818 complex (Norambuena Van Els Muntildeoz- Ramiacuterez amp Victoriano 2018) We ensured a full search of parameter space by assessing models using fixed time parameters at every 1- million- year interval in the tree As a baseline for comparison we also calculated likelihood estimations of a diversity- independent constant- rate birthndashdeath model (function bd_ML) For model comparison we used AIC and the bootstrap likeli-hood ratio test of Etienne Pigot and Phillimore (2016) with 10000 bootstrap replicates We made a lineage- through- time plot of our data using the R package ldquopaleotreerdquo

24emsp|emspModel- based biogeographic analysis

We used the dispersal- vicariance- like (DIVALIKE Ronquist 1997) and Bayesian analysis of biogeography when the number of areas

488emsp |emsp emspensp van ELS Et aL

is large (BAYAREALIKE Landis Matzke Moore amp Huelsenbeck 2013) models in the package BioGeoBears (Matzke 2012) imple-mented in R v320 BioGeoBears optimizes ancestral range states onto internal nodes of a tree and produces likelihood estimates of the transitions between states on these nodes The DIVALIKE model functions in a similar likelihood framework as the dispersalndashextinc-tionndashcladogenesis model (Ree amp Smith 2008) but excludes certain biogeographic scenarios including subset sympatry BAYAREALIKE

finally only allows for events to happen along branches and not at cladogenesis events We constructed a geographic range matrix (adaptation of Cracraft 1985) coding each taxon as present or ab-sent in one or multiple areas We included the following geographic regions in the model Andes lowlands east of the Andes lowlands west of the Andes and the area north of the Panamanian Isthmus (including North America) Varying the maximum number of areas a taxon can occupy from 2 to 4 had little effect on likelihood estimates

TABLE 1emspTaxon sample list including Anthus taxon sampled institution tissue number from tissue collection country region and Genbank accession number per locus Asterisks denote sequences obtained from historical samples Institution codes are as follows AMNH American Museum of Natural History BAS British Antarctic Survey FIMNT Falkland Islands Museum and National Trust KU University of Kansas Natural History Museum KUSNM Danish Natural History Museum at University of Copenhagen LSUMZ Louisiana State University Museum of Natural Science MCZ Museum of Comparative Zoology at Harvard UCCC Universidad de Concepcioacuten USNM Smithsonian Institution National Museum of Natural History UWBM University of Washington Burke Museum and YPM Yale Peabody Museum

Taxon Institution Tissue Country Region ND2 MYO FGB5 ACOI9

antarcticus BAS 2 South Georgia ndash MF320010 MF320015 MF320056 MF320047

antarcticus BAS 3 South Georgia ndash MF320009 MF320016 MF320057 MF320048

bogotensis KUSNM 116859 Ecuador Cotopaxi MF319979 MF320095 MF320070 MF320027

bogotensis LSUMZ 431 Peru Piura MF320026 MF320094 MF320069 MF320026

immaculatus KU 25127 Peru Ayacucho MF320028 MF320105 MF320074 MF320028

meridae AMNH 811977 Venezuela Meacuterida MF320011 ndash ndash ndash

meridae AMNH 811978 Venezuela Meacuterida MF320012 ndash ndash ndash

shiptoni USNM 645734 Argentina Tucumaacuten MF320000 MF320111 MF320080 MF320034

shiptoni UWBM 54394 Argentina Tucumaacuten MF319999 MF320110 MF320079 MF320033

chacoensis AMNH 797085 Argentina Coacuterdoba MF320008 ndash ndash

calcaratus LSUMZ 61430 Peru Puno MF319985 MF320084 MF320051 MF320016

calcaratus LSUMZ 61431 Peru Puno MF319986 MF320085 MF320052 MF320017

catamarcae UWBM 54511 Argentina Tucumaacuten MF320001 MF320012 MF320081 MF320044

chilensis AMNH 13589 Argentina Riacuteo Negro MF320035 MF320100 MF320060 MF320035

chilensis AMNH 13591 Argentina Riacuteo Negro MF320036 MF320101 MF320061 MF320036

correndera USNM 630116 Uruguay Tacuaremboacute MF319989 MF320088 MF320055 MF320020

grayi FIMNT MalvinasFalklands

ndash MF320007 MF320102 MF320071 MF320037

brevirostris KU 21673 Peru Puno MF319996 MF320103 MF320072 MF320038

brevirostris KU 21681 Peru Puno MF319997 MF320104 MF320073 MF320039

furcatus UWBM 54556 Argentina Tucumaacuten MF347705 MF320113 MF320082 MF320045

furcatus USNM 635884 Uruguay Artigas MF320002 MF320114 MF320083 MF320046

brasilianus UWBM 54574 Argentina Corrientes MF319991 MF320090 MF320059 MF320022

brasilianus USNM 630210 Uruguay Tacuarembo MF319990 MF320089 MF320058 MF320021

dabbenei UCCC 2376 Chile Araucania MF320013 MF320117 ndash MF320049

dabbenei UCCC 2377 Chile Araucania MF320014 MF320118 ndash MF320050

hellmayri KU 9813 Argentina Jujuy MF319994 MF320108 MF320077 MF320042

hellmayri UWBM 54528 Argentina Tucumaacuten MF319995 MF320109 MF320078 MF320043

abariensis USNM 626029 Guyana Parabara MF319987 MF320086 MF320053 MF320018

abariensis YPM 13701 Suriname Sipaliwini MF319988 MF320087 MF320054 MF320019

lutescens LSUMZ 87109 Bolivia Santa Cruz MF320003 MF320098 MF320067 MF320029

lutescens USNM 645602 Argentina Tucumaacuten MF320004 MF320099 MF320068 MF320030

parvus LSUMZ 41613 Panama Bocas del Toro

MF319982 MF320093 MF320064 MF320025

(Continues)

emspensp emsp | emsp489van ELS Et aL

We did not apply time stratification or distance multipliers but we ran a separate analysis placing a constraint on adjacency between areas (where east and west of Andes and north and south of the Panamanian Isthmus were considered non- adjacent)

3emsp |emspRESULTS

31emsp|emspPhylogenetic relationships

ND2 was represented by 2921041 variable sites ACOI9 by 62960 FIB5 by 37581 and MYO by 34723 Our species tree (Figure 2 Supporting Information Figure S2 for 95 credibility intervals Supporting Information Figure S3 for single gene trees) obtained using BEAST v 232 reveals a major split between two groups of Anthus One group consists of small- bodied taxa mostly found in the lowlands (A lutescens A furcatus dOrbigny and Lafresnaye 1837 A spraguei A chacoensis Zimmer 1952) with the exception of A brevirostris Taczanowski 1875 The other group contains a mix of Andean and lowland taxa (A hellmayri Hartert 1909 A bogotensis Sclater 1855 A correndera A nattereri Sclater 1878) A peruvianus Nicholson 1878 (traditionally a subspecies of A lutescens) is sister to this group For further discussion of taxonomy we refer to Van Els and Norambuena (2018) Notice that the best tree reported in this study differs slightly from Van Els and Norambuena (2018) because we used a more appropriate tree prior and a longer MCMC chain

32emsp|emspTiming and diversification

According to our BEAST v 232 analysis the ancestor of New World Anthus is estimated to have evolved ~75 Mya and subsequently diver-sified mainly on the South American continent (Figures 2 and 3) where the main biogeographic split took place in the early Pliocene between mainly lowland and Andean taxa More recent speciation events are mainly associated with tips that are related to an Andean state

The diversity- dependent model with a parameter shift at ~58 Mya (Table 2) was the most likely model according to AICw

and the second most likely model had a shift at ~18 Mya Likelihood bootstrap analyses indicate that although our LTT plots (Figure 4) and diversification analyses show a shift in dynamics at these points in geological time the size of our phylogenetic tree likely prevents us from finding statistical support at α = 005 (Figure 5)

33emsp|emspBiogeography

BioGeoBears revealed the DECc model was most likely (Table 3) Dispersal (d) and extinction (e) events are both of importance accord-ing to this model with a relatively large role for dispersal and extinc-tion compared to other models BioGeoBears allocates the oldest node in the tree (basal node) with highest likelihood to uncertain geographic origin (Figure 2) The subsequent splits in the two main clades within the group are most likely between an Andean origin for A bogotensis meridaeA b bogotensisA hellmayri and an eastern lowland origin for the small- bodied subclade with a preceding split of A peruvianus occurring on the Pacific coast of South America

There is likely at least one lowland- to- Andes dispersal event (A furcatusA brevirostris) and two Andes- to- lowland dispersal events (A hellmayri brasilianusA h hellmayri and split between lowland and Andean A correndera) Several taxa speciated within the Andes the first split occurred between the northern Andean A b meridae and the other taxa followed by diversification between the northern and relatively isolated southern Andes (A b shiptoni A h dabbenei)

4emsp |emspDISCUSSION

41emsp|emspMiocene grassland development likely spurred Anthus diversification

Lineage- through- time analysis shows an increase in Anthus line-ages starting at the end of the Miocene and beginning of Pliocene Diversification analysis showed the most likely model is one of shifting diversification rates at 58 Mya although a power analysis failed to reject constant rates at that time probably as a result of

Taxon Institution Tissue Country Region ND2 MYO FGB5 ACOI9

peruvianus LSUMZ 44804 Peru La Libertad MF319984 MF320097 MF320066 MF320032

peruvianus LSUMZ 48218 Peru Lima MF319983 MF320096 MF320065 MF320031

nattereri KU 3604 Paraguay Itapuacutea MF319992 MF320106 MF320075 MF320040

nattereri KU 3665 Paraguay Itapuacutea MF319993 MF320107 MF320076 MF320041

spraguei LSUMZ 25702 USA North Dakota

MF319980 MF320091 MF320062 MF320023

spraguei LSUMZ 21749 USA Louisiana MF319981 MF320092 MF320063 MF320024

cinnamomeus UWBM 52816 South Africa Eastern Cape AY329410 ndash ndash ndash

gustavi UWBM 75556 Russia Primorsky Krai

HM538396 ndash ndash ndash

rubescens LSU 53141 USA California MF320015 ndash ndash ndash

rufulus FMNH 358350 Philippines Sibuyan KP671566 ndash ndash ndash

TABLE 1emsp (Continued)

490emsp |emsp emspensp van ELS Et aL

the relatively small number of tips in our tree The shift in diversi-fication rates reflects the start of the diversification of Anthus on the South American continent which coincided with or occurred right after the formation of C4 grasslands (Latrubesse et al 2010) and much after the completion of C3 grasslands (Stroumlmberg 2011) It is noteworthy that many other grassland- adapted taxa of South American origins such as Alectrurus and Muscisaxicola flycatchers (Fjeldsaring Ohlson Batalha- Filho Ericson amp Irestedt 2018) and fur-nariids of the genera Cinclodes and Asthenes (Derryberry et al 2011) originated in the Pliocene or later even though other related subos-cines from other habitats diversified much earlier Anthus may have experienced an ldquoearly burstrdquo of diversification (Simpson 1953) after its arrival to South Americas grasslands at a time when most pas-serines of Neotropical origins had not yet experienced such a burst in this habitat

The sister lineage to the New World Anthus is Eurasian (Alstroumlm et al 2015 Voelker 1999ab) Voelker (1999a) suggested that dis-persal occurred via the Bering Strait A spraguei is the only North American member of the clade and this taxon likely dispersed from South to North America (in agreement with Voelker 1999b) As far as we are aware no fossils of Anthus are known from Central America ManyMexicangrasslandsdatefromtheTertiary(Rzedọwski1975)

and it is curious that the Mexican and Central American grasslands (north of Panama) are devoid of resident Anthus especially because other grassland taxa such as Cistothorus (Robbins amp Nyaacuteri 2014) and Sturnella (Barker Vandergon amp Lanyon 2008) occur through-out the region The paucity of North and Central American Anthus pertaining to our New World clade probably indicates that in re-sponse to climate- associated habitat alterations associated with reductions in short- stature grassland Anthus retracted its range in the region (cf Voelker 1999b) It could also indicate that a long- distance dispersal event from Asia to South America rather than arrival via a Bering Sea crossing resulted in the colonization of the New World by Anthus This hypothesis is not as far- fetched as it may seem given that that long- distance dispersal from Asia to South America is known to occur at least occasionally in Anthus (Brinkhuizen et al 2010) Long- distance dispersal and subsequent diversification are known in Motacillidae from other regions as well Alstroumlm et al (2015) suggest that two members of the family estab-lished populations in their isolated African and Wallacean winter quarters and evolved into morphologically and ecologically highly divergent taxa

Given our phylogeny the Neotropical ancestral Anthus has unknown geographic origins within the New World An ances-tral Anthus arrived to South America prior to the closure of the Isthmus of Panama and not long after the formation of C4 grass-lands during the Miocene (Latrubesse et al 2010) The topology of our tree may provide some insight into the evolutionary origins of the subsequent split between the two major Neotropical sub-clades of Anthus The first major split possibly arose due to an an-cestral Anthus being isolated between the Andes and the eastern lowlands (as our biogeographic analysis suggests) or on either side of the Andes Given that high- Andean grasslands were mostly not yet formed at the time of this split we suggest the latter is a more likely option The biogeographic analysis may have been affected by the little weight of the single lineage associated with A peruvianus Some of the deepest branches in our tree such as that of A peru-vianus are represented by taxa not included in Voelker (1999ab) These deep branches have a relatively large potential to subdivide shorter branches or groups and are thus comparatively informative (Wiens 2006) Indeed our recovery of phylogenetic relationships the estimation of timing of diversification and the determination of dispersal patterns in Neotropical Anthus have been enabled by the sampling of relatively rare taxa that remained un- sampled in earlier decades

42emsp|emspThe Andes stimulated recent diversification

Our lineage- through- time plot shows a period of stasis in diversifi-cation preceding the Pleistocene followed by an increasing accu-mulation of lineages during the late Pleistocene This is supported by our second most likely diversification model indicating a shift in diversity dynamics ~17ndash18 Mya Most of the new lineages respon-sible for the uptick in diversification toward the present are Andean rather than lowland in origin Although we lack exact data on the

F IGURE 1emspSampling map of Neotropical Anthus A lutescens (white circles) A peruvianus (black circles) A bogotensis (stars) A furcatus and A brevirostris (ovals) A hellmayri (squares) A correndera (rectangles) A chacoensis (hatch) and A nattereri (cross) Background shade represents taxon diversity darker being more taxa

emspensp emsp | emsp491van ELS Et aL

development of Andean habitats in relation to orogeny it seems clear that large expanses of the highest vegetation zones probably developed during the last ~45 Mya of most intense orogeny (Hoorn et al 2010 Madrintildeaacuten Corteacutes amp Richardson 2013 Vuilleumier 1969) and continue to the present (Madrintildeaacuten et al 2013) Among Neotropical Anthus there are four groups of sister lineages repre-sented sympatrically in both lowlands and highlands indicating that similar patterns of niche partitioning occurred at low and high eleva-tions Neotropical Anthus species seem to be flexible to changes in abiotic conditions associated with a high- montane versus lowland lifestyle because dispersal has taken place in both the upslope and downhill directions Whether or not the southern Andes where grasslands occur lower down than in the more tropical northern Andes have served as a stepping stone between lowland and alpine populations remains a question

Although Anthus mostly colonized the Andes before the Pleistocene most of the within- Andes diversification seems to have occurred during the last 2 Mya in line with evidence that Andean birds in general show an uptick in diversification during the Pleistocene (Weir 2006) as well as Andean grassland- inhabiting organisms such as Cistothorus (wrens Robbins amp Nyaacuteri 2014) Muscisaxicola (flycatchers Fjeldsaring et al 2018) Hypericum (St Johns worts Nuumlrk Scheriau amp Madrintildeaacuten 2013) and Lupinus (lupines Hughes amp Eastwood 2006) The formation of Andean ldquoislandsrdquo with the completion of isolated high peaks likely contributed to the di-versification of these taxa (Cuervo 2013) as did the formation of Andean glaciers severing populations (Vuilleumier amp Simberloff 1980)

F IGURE 2emspBiogeography and diversification of Neotropical Anthus plotted on consensus tree based on ND2 MYO FIB5 and ACOI9 genes Pie charts indicate ancestral range states at each node according to DECc model in BioGeoBears blue lowlands south of the Amazon Basin and east of Andes green is Andes yellow is lowlands north of Amazon Basin and area north of Isthmus of Panama red represents the Peruvian coastal strip and other colors are uncertain states (also see inset map) Values at node represent posterior support (above) and bootstrap likelihood (below) Values at bottom of tree indicate geological time in millions of years For node bars indicating temporal uncertainty see appendix 2 Correndera lowlands include A c correnderachilensisgrayiantarcticus and correndera Andes represents A c catamarcaecalcaratus Tips may represent gt1 individual in which case they were collapsed Pipit illustration Tyler 2004

10100

09897

09593

09393

09896

09185

09999

099100

10100

10100

10100

10100

10100

09797 10

100

10100

spragueibrevirostrisfurcatus

chacoensis

lutescensparvus

brasilianushellmayrimeridaecorrendera Andescorrendera lowlandsnattereriperuvianus

bogotensis shiptoni

immaculatusdabbenei

F IGURE 3emspBiogeography of Neotropical Anthus Arrows indicate putative dispersal events dashed arrows are uncertain dispersal routes and numbers are putatively associated divergence times in Mya Colors of areas agree with those used in biogeographic analyses Dashed lines indicate intra- Andean barriers to dispersal

492emsp |emsp emspensp van ELS Et aL

43emsp|emspSpeciation in the tropical lowlands precedes the LGM

Anthus is represented by only one lineage in the South American lowlands north of the Amazon River (A l parvus (populations cur-rently often classified as A l lutescens north of the river subsumed in A l parvus here see Van Els amp Norambuena 2018)) During the last 1 Mya a split occurred between populations of A lutes-cens in the north and south of the Amazon Basin Although several landscape- level processes may have led to this split it is probable that the transformation of the South American landscape from a ldquocratonicrdquo (based on geologically stable shield formations) to an Andean- dominated system (Hoorn et al 2010) contributed to landscape changes (mainly spread of forest and other mesic habi-tats) in and around the Amazon Basin that led to isolation of both groups According to the refuge hypothesis (Haffer 1969) the late Pleistocene lowland South American landscape should have been one of extensive open habitats sprinkled with pockets of forest Under this scenario we would expect lineages associated with tropical grasslands to expand their distributions across the rela-tively dry Amazon Basin LGM expansion of the dry biome would have likely caused a connection between northern and southern

Amazonian populations and subsequent exchange of genes in re-cent history The post- LGM retraction of open habitats toward the margins of the Basin would again increase genetic isolation but would at best cause shallow divergences between open- country lineages There is no increase in the number of lowland lineages during the late Pleistocene and the divergence between northern and southern populations of A lutescens precedes the LGM con-tradicting the refugium theory The older origins of this split agrees with older splits found in many forest- based taxa (Patel et al 2011 Ribas Aleixo Nogueira Miyaki amp Cracraft 2012) suggest-ing one of the many alternative theories explaining Amazonian spe-ciation (Arruda et al 2017 Burkart 1975 Bush amp Oliveira 2006 Colinvaux 1998 Patel et al 2011) Only A lutescens and to a lim-ited extent A nattereri occur exclusively in the tropical lowlands which may be caused by ecological or physiological limits to the expansion of Anthus into tropical lowland grasslands

A number of other bird species have a similar distribution pat-tern north and south of the Amazon (circum- Amazonian distribution a similar pattern found in many African savanna birds distributed around the Congo Basin Remsen et al 1991) and further investi-gation should reveal whether (a) northern populations are generally derived from southern populations and whether (b) the timing of the

F IGURE 4emspLineages- through- time plot of the Neotropical Anthus clade Black line is the number of lineages minus subspecies- level lineages in A correndera (cf Figure 2) and gray represents confidence interval Dashed lines from left to right represent late MiocenePliocene boundary and associated completion of spread of lowland grasslands lower bound on uppermost Andean vegetation zones upper bound on uppermost Andean vegetation zones and the start of Quaternary glaciations

TABLE 2emspOutput of tests for diversity- dependent diversification in package DDD CR = constant rates DD = diversity- dependent SR = shifting rates (number indicates time of shift) k = number of parameters max log lik = maximum log likelihood of model AICw = Akaike information criterion weights λ = speciation rate μ = extinction rate K = clade- level carrying capacity (after 1 first and 2 second shift in case of a SR model) tshift = time at which shift occurs in diversity dynamics (in case of SR model) An asterisk indicates the most likely model

Model k max log lik AICw λ μ K1 K2 tshift

CR 2 minus34697 0000 0269 0001 ndash ndash ndash

DD 3 minus31504 0021 2047 0324 16577 ndash ndash

SR 5 minus28377 0065 1157 0001 8999 19489 1682

SR58 5 minus25874 0791 9542 0344 1273 16386 5856

SR53 4 minus31257 0009 1639 0326 94784 16613 5300

SR40 4 minus31381 0009 2211 0301 13855 16516 4000

SR20 4 minus31141 0011 1549 0156 11544 17171 2000

SR18 4 minus29021 0092 1097 0001 8999 19641 1800

emspensp emsp | emsp493van ELS Et aL

split is similar to that found in A lutescens Taxa occurring in grass-lands north of the Amazon are generally a subset of those occur-ring in southern South America with few endemic representatives (Stotz Fitzpatrick Parker amp Moskovits 1996 eg Tyrannidae and Thraupidae) The relatively modest extent of grasslands north of the Amazon relative to southern South America may explain this pattern to some extent Grasslands located in the north of the Amazon Basin were colonized much later according to our biogeographic analy-ses resulting in a discrepancy in diversity This pattern is not always shared by other Neotropical grassland taxa (see Campagna Silveira Tubaro amp Lougheed 2013) for which Pleistocene landscape pertur-bations may have driven rapid speciation in southern South American grasslands (Lijtmaer Sharpe Tubaro amp Lougheed 2004) Regardless of the mechanism driving these diversity patterns southern South America seems to be a center of diversification for Neotropical low-land grassland birds

44emsp|emspShort- distance gene flow and long- distance isolation

The DECc model of biogeography was most likely outperforming both DIVALIKE and BAYAREALIKE models which in cases where a taxon can occupy a maximum of four areas simultaneously is most

likely due to a lack of subset sympatry (Matzke 2014) In other words the evolution of sister species is not likely to happen sympatrically testimony to the fact that gene flow may hinder diversification over shorter distances or in the absence of considerable vicariant effects Having constraints on the adjacency of areas improves the likeli-hood of the model which shows that direct biogeographic events

F IGURE 5emspBootstrap likelihood ratio test for Anthus diversification analysis in DDD Distribution of logarithms of the likelihood ratio generated in DDD under an (a) constant- rate (CR) model for diversity dependence (b) a diversity- dependent model (DD) (c) a constant- rate model for shifting rates and (d) a shifting rate (SR) model using the parameters of the best SR model in Table 2 to test for effects of diversity dependence Crosses represent values of the likelihood ratio for the real data and circles represent values of the likelihood ratio for a significance level of α = 005 with 10000 replicates

TABLE 3emspResults ancestral range estimation analyses from BioGeoBears using no constraints on adjacency of four defined biogeographic areas (first six rows) and using constraints on adjacency between areas east and west of Andes and between north and south of Panamanian Isthmus (last six rows) df is degrees of freedom per model LnL is log likelihood AICw is weight of Akaike information criterion d is dispersal e is extinction and an asterisk indicates the most likely model

Model df minusLnL AICw d e

DEC 2 30724 0001 0032 0035

DIVALIKE 2 25942 0008 0031 0000

BAYAREALIKE 2 38794 0001 0033 0222

DECc 2 21080 0985 0120 2005

DIVALIKEc 2 25942 0008 0030 0000

BAYAREALIKEc 2 38733 0001 0064 0095

494emsp |emsp emspensp van ELS Et aL

between areas on either side of the Andes and the Panamanian Isthmus are unlikely

Biogeographic models including founder event speciation have been found to explain biogeographic patterns in island systems (Matzke 2014 Paulay amp Meyer 2002) but are also common in some terrestrial settings (Matzke 2013) Founder event speciation may also play a role in our system However the use of the ldquojrdquo pa-rameter in biogeographic models has been criticized recently (Ree amp Sanmartiacuten 2018) because of the tendency of models includ-ing ldquojrdquo to underestimate non- jump dispersal events at ancestral nodes Also statistical comparison to models excluding the jump dispersal parameter is not valid due to non- equivalency issues An alternative to test for effects of jump dispersal would be to use a method to assess state- dependent lineage diversification that appropriately addresses Type I error issues often associated with these methods (eg HiSSE Beaulieu amp OMeara 2016 SecSSE Herrera- Alsina van Els amp Etienne 2018) We consider sample size in our study to be insufficient for such relatively parameter- rich analyses

ACKNOWLEDG MENTS

We thank the following institutions and their staff for providing samples Paul Sweet (AMNH) Nate Rice (ANSP) Stephen Massam (FIMNT) John Bates and Ben Marks (FMNH) Krzysztof Zyskowski (YPM) Mark Robbins (KU Biodiversity Institute) Sharon Birks and John Klicka (UWBM) Brian Schmidt (USNM Smithsonian) Jon Fjeldsaring and Jan Bolding Kristensen (ZMUC) Jeremiah Trimble (MCZ) Kimball Garrett (LACM) Pablo Tubaro and Dariacuteo Lijtmaer (MACN) Alexandre Aleixo (MPEG) Jorge Peacuterez- Emaacuten at the Instituto de Zoologiacutea Tropical at the Universidad Central de Venezuela and Pedro Victoriano at the Universidad de Concepcioacuten in Chile Andy Wood at the British Antarctic Survey provided valua-ble samples of A c antarcticus Sabrina Taylor at LSUs Department of Renewable Natural Resources kindly allowed me to work in her ancient DNA laboratory James V Remsen Jr and Robb Brumfield kindly reviewed the manuscript Funding was provided by the LSU Museum of Natural Science Birdathon Fund the Stichting PA Hens Memorial Fund an American Ornithologistsrsquo Union Alexander Wetmore Memorial Research Award and the American Museum of Natural History Frank M Chapman Memorial Fund PVE thanks the Faculty of Science and Engineering and the Groningen Institute for Evolutionary Life Sciences at the University of Groningen for funding through the Adaptive Life Program HVN is grateful for the CONICYT- PCHADoctoradoNacional2013- 21130354 schol-arship RSE thanks the Netherlands Organization for Scientific Research (NWO) for financial support through a VICI grant

ORCID

Paul van Els httpsorcidorg0000-0002-9499-8873

Heraldo V Norambuena httpsorcidorg0000-0003-0523-3682

R E FE R E N C E S

Agarwal I amp Ramakrishnan U (2017) A phylogeny of open- habitat liz-ards Squamata Lacertidae Ophisops supports the antiquity of Indian grassy biomes Journal of Biogeography 44 2021ndash2032 httpsdoiorg101111jbi12999

Alstroumlm P Joslashnsson K A Fjeldsaring J Oumldeen A Ericson P G amp Irestedt M (2015) Dramatic niche shifts and morphological change in two insular bird species Royal Society Open Science 2 140ndash364 httpsdoiorg101098rsos140364

Arruda D M Schaefer C E Fonseca R S Solar R R amp Fernandes-Filho E I (2017) Vegetation cover of Brazil in the last 21 ka New insights into the Amazonian refugia and Pleistocenic arc hypotheses Global Ecology and Biogeography 27 47ndash56 httpsdoiorg101111geb12646

Barker F K Vandergon A J amp Lanyon S M (2008) Assessment of species limits among yellow- breasted meadowlarks Sturnella spp using mitochondrial and sex- linked markers The Auk 125 869ndash879 httpsdoiorg101525auk200807148

Bates J M Tello J G amp Silva J M C (2003) Initial assessment of genetic diversity in ten bird species of South American Cerrado Studies on Neotropical Fauna and Environment 38 87ndash94 httpsdoiorg101076snfe3828715924

Beaulieu J M amp OMeara B C (2016) Detecting hidden diversification shifts in models of trait- dependent speciation and extinction Systematic Biology 65 583ndash601 httpsdoiorg101093sysbiosyw022

Brinkhuizen D Brinkhuizen L Keaveney A amp Jane S (2010) Red- throated Pipit Anthus cervinus a new species for South America Cotinga 32 15ndash17 httpsdoiorg10116017365

Burkart A (1975) Evolution of grasses and grasslands in South America Taxon 24 53ndash66 httpsdoiorg1023071219001

Bush M B amp Oliveira P E D (2006) The rise and fall of the Refugial Hypothesis of Amazonian speciation a paleoecological perspective Biota Neotropica 6 httpsdoiorg101590S1676

Campagna L Silveira L F Tubaro P L amp Lougheed S C (2013) Identifying the sister species to the rapid capuchino radiation (Passeriformes Sporophila) The Auk 130 645ndash655 httpsdoiorg101525auk201313064

Claramunt S Derryberry E P Remsen J V amp Brumfield R T (2012) High dispersal ability inhibits speciation in a continental radiation of passerine birds Proceedings of the Royal Society of London B Biological Sciences 279 1567ndash1574 httpsdoiorg101098rspb20111922

Colinvaux P (1998) A new vicariance model for Amazonian endemics Global Ecology amp Biogeography Letters 7 95ndash96

Cracraft J (1985) Historical biogeography and patterns of dif-ferentiation within the South American avifauna Areas of en-demism Ornithological Monographs 36 49ndash84 httpsdoiorg10230740168278

Cuervo A M (2013) Evolutionary assembly of the Neotropical montane avifauna Unpublished Dissertation Louisiana State University Baton Rouge LA

Darriba D Taboada G L Doallo R amp Posada D (2012) jModelT-est 2 more models new heuristics and parallel computing Nature Methods 9 772 httpsdoiorg101038nmeth2109

Derryberry E P Claramunt S Derryberry G Chesser R T Cracraft J Aleixo A hellip Brumfield R T (2011) Lineage diversi-fication and morphological evolution in a large- scale continental radiation the Neotropical ovenbirds and woodcreepers (Aves Furnariidae) Evolution 65 2973ndash2986 httpsdoiorg101111j1558-5646201101374x

Diamond J M Gilpin M E amp Mayr E (1976) Species- distance rela-tion for birds of the Solomon Archipelago and the paradox of the great speciators Proceedings of the National Academy of Sciences 73 2160ndash2164 httpsdoiorg101073pnas7362160

Dmitriev D A amp Rakitov R A (2008) Decoding of superimposed sub-species produced by direct sequencing of heterozygous indels PLoS

emspensp emsp | emsp495van ELS Et aL

Computational Biology 4 e1000113 httpsdoiorg101371jour-nalpcbi1000113

Drummond A J amp Rambaut A (2007) BEAST Bayesian evolutionary analysis by sampling trees BMC Evolutionary Biology 7 214 httpsdoiorg1011861471-2148-7-214

Edwards E J Osborne C P Stroumlmberg C A amp Smith S A (2010) The origins of C4 grasslands integrating evolutionary and eco-system science Science 328 587ndash591 httpsdoiorg101126science1177216

Emslie S D (2007) Fossil passerines from the early Pliocene of Kansas and the evolution of songbirds in North America The Auk 124 85ndash95 httpsdoiorg1016420004-8038(2007)124[85FPFTEP]20CO2

Estep M C McKain M R Diaz D V Zhong J Hodge J G Hodkinson T R hellip Kellogg E A (2014) Allopolyploidy diversification and the Miocene grassland expansion Proceedings of the National Academy of Sciences 111 15149ndash15154 httpsdoiorg101073pnas1404177111

Etienne R S amp Haegeman B (2012) A conceptual and statistical frame-work for adaptive radiations with a key role for diversity dependence The American Naturalist 180 75ndash89 httpsdoiorg101086667574

Etienne R S Pigot A L amp Phillimore A B (2016) How reliably can we infer diversity- dependent diversification from phyloge-nies Methods in Ecology and Evolution 7 1092ndash1099 httpsdoiorg1011112041-210X12565

Eva H D Belward A S De Miranda E E Di Bella C M Gond V Huber O hellip Fritz S (2004) A land cover map of South America Global Change Biology 10 731ndash744 httpsdoiorg101111j1529-8817200300774x

Fernandes A Cohn-Haft M Hrbek T amp Farias W E (2015) Rivers acting as barriers for bird dispersal in the Amazon Revista Brasileira de Ornitologia 22 361ndash371

Fjeldsaring J Bowie R C amp Rahbek C (2012) The role of mountain ranges in the diversification of birds Annual Review of Ecology Evolution and Systematics 43 249ndash265 httpsdoiorg101146annurev-ecolsys-102710-145113

Fjeldsaring J Ohlson J I Batalha-Filho H Ericson P G amp Irestedt M (2018) Rapid expansion and diversification into new niche space by fluvicoline flycatchers Journal of Avian Biology 49 jav-01661 httpsdoiorg101111jav01661 httpsdoiorg101111jav01661

Guindon S amp Gascuel O (2003) A simple fast and accurate algorithm to estimate large phylogenies by maximum likelihood Systematic Biology 52 696ndash704 httpsdoiorg10108010635150390235520

Haffer J (1969) Speciation in Amazonian forest birds Science 165 131ndash137 httpsdoiorg101126science1653889131

Harvey M G amp Brumfield R T (2015) Genomic variation in a wide-spread Neotropical bird Xenops minutus reveals divergence popula-tion expansion and gene flow Molecular Phylogenetics and Evolution 83 305ndash316 httpsdoiorg101016jympev201410023

Herrera-Alsina L van Els P amp Etienne R S (2018) Detecting the dependence of diversification on multiple traits from phylogenetic trees and trait data Systematic Biology 68(2) 317ndash328

Heslewood M M Elphinstone M S Tidemann S C amp Baverstock M R (1998) Myoglobin intron variation in the Gouldian Finch Erythrura gouldiae assessed by temperature gradient gel elec-trophoresis Electrophoresis 19 142ndash151 httpsdoiorg101002elps1150190203

Hoorn C Wesselingh F P Ter Steege H Bermudez M A Mora A Sevink J hellip Antonelli A (2010) Amazonia through time Andean uplift climate change landscape evolution and biodiversity Science 330 927ndash931 httpsdoiorg101126science1194585

Hovick T J Elmore R D amp Fuhlendorf S D (2014) Structural het-erogeneity increases diversity of non- breeding grassland birds Ecosphere 5 1ndash13 httpsdoiorg101890ES14-000621

Hughes C amp Eastwood R (2006) Island radiation on a continental scale exceptional rates of plant diversification after uplift of the

Andes Proceedings of the National Academy of Sciences 103 10334ndash10339 httpsdoiorg101073pnas0601928103

Kearse M Moir R Wilson S Stones-Havas S Cheung M Sturrock S hellip Drummond A (2012) Geneious Basic an integrated and ex-tendable desktop software platform for the organization and anal-ysis of sequence data Bioinformatics 28 1647ndash1649 httpsdoiorg101093bioinformaticsbts199

Kimball R T Braun E L Barker F K Bowie R C Braun M J Chojnowski J L hellip Yuri T (2009) A well- tested set of prim-ers to amplify regions spread across the avian genome Molecular Phylogenetics and Evolution 50 654ndash660 httpsdoiorg101016jympev200811018

Kumar S Nei M Dudley J amp Tamura K (2008) MEGA a biologist- centric software for evolutionary analysis of DNA and protein sequences Briefings in Bioinformatics 9 299ndash306 httpsdoiorg101093bibbbn017

Landis M J Matzke N J Moore B R amp Huelsenbeck J P (2013) Bayesian analysis of biogeography when the number of areas is large Systematic Biology 62 789ndash804 httpsdoiorg101093sysbiosyt040

Latrubesse E M Cozzuol M da Silva-Caminha S A F Rigsby C A Absy M L amp Jaramillo C (2010) The Late Miocene paleogeog-raphy of the Amazon Basin and the evolution of the Amazon River system Earth Science Review 99 99ndash124 httpsdoiorg101016jearscirev201002005

Lees A C amp VanderWerf E A (2011) First record of Blyths Pipit Anthus godlewskii for Micronesia Bulletin of the British Ornithological Club 131 212ndash217

Lerner H R Meyer M James H F Hofreiter M amp Fleischer R C (2011) Multilocus resolution of phylogeny and timescale in the ex-tant adaptive radiation of Hawaiian honeycreepers Current Biology 21 1838ndash1844 httpsdoiorg101016jcub201109039

Lijtmaer D A Sharpe N M Tubaro P L amp Lougheed S C (2004) Molecular phylogenetics and diversification of the genus Sporophila (Aves Passeriformes) Molecular Phylogenetics and Evolution 33 562ndash579 httpsdoiorg101016jympev200407011

Little W E T Hockey P A amp Jansen R (2013) A burning issue fire overrides grazing as a disturbance driver for South African grassland bird and arthropod assemblage structure and diversity Biological Conservation 158 258ndash270 httpsdoiorg101016jbiocon201209017

Lovette W E J (2005) Glacial cycles and the tempo of avian speciation Trends in Ecology and Evolution 20 57ndash59 httpsdoiorg101016jtree200411011

Madrintildeaacuten S Corteacutes A J amp Richardson J E (2013) Paacuteramo is the worlds fastest evolving and coolest biodiversity hotspot Frontiers in Genetics 4 192 httpsdoiorg103389fgene201300192

Matzke N J (2012) Founder- event speciation in BioGeoBears package dramatically improves likelihoods and alters parameter inference in dispersalndashextinctionndashcladogenesis DEC analyses Frontiers of Biogeography 4 210

Matzke N J (2013) Probabilistic historical biogeography new models for founder- event speciation imperfect detection and fossils allow improved accuracy and model- testing Frontiers of Biogeography 5 242ndash248

Matzke N J (2014) Model selection in historical biogeography reveals that founder- event speciation is a crucial process in island clades Systematic Biology 63 951ndash970 httpsdoiorg101093sysbiosyu056

Mild K amp Alstroumlm P (2010) Pipits and Wagtails of Europe Asia and North America London UK AC Black

Neiswenter S A amp Riddle B R (2010) Diversification of the Perognathus flavus species group in emerging arid grasslands of west-ern North America Journal of Mammalogy 91 348ndash362 httpsdoiorg10164409-MAMM-A-1021

496emsp |emsp emspensp van ELS Et aL

Norambuena H V Van Els P Muntildeoz-Ramiacuterez C P amp Victoriano P F (2018) First steps towards assessing the evolutionary history and phylogeography of a widely distributed Neotropical grassland bird (Motacillidae Anthus correndera) PeerJ 6 e5886 httpsdoiorg107717peerj5886

Nuumlrk N M Scheriau C amp Madrintildeaacuten S (2013) Explosive radiation in high Andean Hypericummdashrates of diversification among New World lineages Frontiers in Genetics 4 175 httpsdoiorg103389fgene201300175

Patel S Weckstein J D Pataneacute J S Bates J M amp Aleixo A (2011) Temporal and spatial diversification of Pteroglossus aracaris (Aves Ramphastidae) in the Neotropics constant rate of diversification does not support an increase in radiation during the Pleistocene Molecular Phylogenetics and Evolution 58 105ndash115 httpsdoiorg101016jympev201010016

Paulay G amp Meyer C (2002) Diversification in the tropical Pacific comparisons between marine and terrestrial systems and the impor-tance of founder speciation Integrative and Comparative Biology 42 922ndash934 httpsdoiorg101093icb425922

Pennington R T amp Hughes C E (2014) The remarkable congruence of New and Old World savanna origins New Phytologist 204 4ndash6 httpsdoiorg101111nph12996

Phillimore A B Freckleton R P Orme C D L amp Owens I P (2006) Ecology predicts large- scale patterns of phylogenetic diversifica-tion in birds The American Naturalist 168 220ndash229 httpsdoiorg101086505763

Pietersen D W Mckechnie A E Jansen R Little I T amp Bastos A D S (2018) Multi- locus phylogeny of African pipits and longclaws (Aves Motacillidae) highlights taxonomic inconsistencies Ibis in press

Ree R H amp Sanmartiacuten I (2018) Conceptual and statistical problems with the DEC+ J model of founder- event speciation and its com-parison with DEC via model selection Journal of Biogeography 45 741ndash749 httpsdoiorg101111jbi13173

Ree R H amp Smith S A (2008) Maximum likelihood inference of geographic range evolution by dispersal local extinction and cladogenesis Systematic Biology 57 4ndash14 httpsdoiorg10108010635150701883881

Remsen J V Areta J I Cadena C D Claramunt S Jaramillo A Pacheco J F hellip Zimmer K J Version (2018) A classification of the bird species of South America American Ornithologistsrsquo Union httpwwwmuseumlsuedu~RemsenSACCBaselinehtm

Remsen J V Rocha O Schmitt C G amp Schmitt D C (1991) Zoogeography and geographic variation of Platyrinchus mystaceus in Bolivia and Peru and the circum- Amazonian distribution pattern Ornitologia Neotropical 2 77ndash83

Ribas C C Aleixo A Nogueira A C Miyaki C Y amp Cracraft J (2012) A palaeobiogeographic model for biotic diversification within Amazonia over the past three million years Proceedings of the Royal Society B 279 681ndash689 httpsdoiorg101098rspb20111120

Robbins M B amp Nyaacuteri Aacute S (2014) Canada to Tierra del Fuego species limits and historical biogeography of the Sedge Wren (Cistothorus platensis) The Wilson Journal of Ornithology 126 649ndash662 httpsdoiorg10167613-1621

Romaacuten-Cuesta R M Carmona-Moreno C Lizcano G New M Silman M Knoke T hellip Vuille M (2014) Synchronous fire activity in the tropical high Andes an indication of regional climate forc-ing Global Change Biology 20 1929ndash1942 httpsdoiorg101111gcb12538

Ronquist F (1997) Dispersal- vicariance analysis a new approach to the quantification of historical biogeography Systematic Biology 46 195ndash203 httpsdoiorg101093sysbio461195

Rzedọwski J (1975) An ecological and phytogeographical analy-sis of the grasslands of Mexico Taxon 24 67ndash80 httpsdoiorg1023071219002

Simpson G G (1953) The major features of evolution New York NY Columbia Univ Press

Smith B T McCormack J E Cuervo A M Hickerson M J Aleixo A Cadena C D hellip Brumfield R T (2014) The drivers of tropical spe-ciation Nature 515 406ndash409 httpsdoiorg101038nature13687

Stephens M amp Donnelly P (2003) A comparison of Bayesian meth-ods for haplotype reconstruction from population genotype data The American Journal of Human Genetics 73 1162ndash1169 httpsdoiorg101086379378

Stotz D F Fitzpatrick J W Parker T A III amp Moskovits D K (1996) Neotropical birds ecology and conservation Chicago IL University of Chicago Press

Stroumlmberg C A (2011) Evolution of grasses and grassland ecosystems Annual Review of Earth and Planetary Sciences 39 517ndash544 httpsdoiorg101146annurev-earth-040809-152402

Tyler S (2004) Paramo Pipit Anthus bogotensis In J del Hoyo A Elliott J Sargatal D A Christie amp E de Juana (Eds) Handbook of the birds of the world alive Barcelona Lynx Edicions

Van Els P amp Norambuena H V (2018) A revision of species limits in Neotropical pipits Anthus based on multilocus genetic and vocal data Ibis 160 158ndash172 httpsdoiorg101111ibi12511

Voelker G (1999a) Molecular evolutionary relationships in the avian genus Anthus Pipits Motacillidae Molecular Phylogenetics and Evolution 11 84ndash94 httpsdoiorg101006mpev19980555

Voelker G (1999b) Dispersal vicariance and clocks historical bio-geography and speciation in a cosmopolitan passerine genus Anthus Motacillidae Evolution 53 1536ndash1552 httpsdoiorg101111j1558-5646

Voelker G (2001) Morphological correlates of migratory distance and flight display in the avian genus Anthus Biological Journal of the Linnean Society 73 425ndash435 httpsdoiorg101111j1095-83122001tb01371x

Vuilleumier F (1969) Pleistocene speciation in birds living in the high Andes Nature 223 1179ndash1180 httpsdoiorg1010382231179a0

Vuilleumier F amp Simberloff D (1980) Ecology versus history as de-terminants of patchy and insular distributions in high Andean birds In M K Hecht W C Steere amp B Wallace (Eds) Evolutionary bi-ology Vol 12 (pp 235ndash379) New York NY Plenum httpsdoiorg101007978-1-4615-6959-6

Weir J T (2006) Divergent timing and patterns of species accumulation in lowland and highland Neotropical birds Evolution 60 842ndash855 httpsdoiorg101111j0014-38202006tb01161x

Wiens J J (2006) Missing data and the design of phylogenetic anal-yses Journal of Biomedical Informatics 39 34ndash42 httpsdoiorg101016jjbi200504001

SUPPORTING INFORMATION

Additional supporting information may be found online in the Supporting Information section at the end of the article

How to cite this article van Els P Norambuena HV Etienne RS From pampa to puna Biogeography and diversification of a group of Neotropical obligate grassland birds (Anthus Motacillidae) J Zool Syst Evol Res 201957485ndash496 httpsdoiorg101111jzs12278