From pampa to puna
van Els, Paul; Norambuena, Heraldo V.; Etienne, Rampal S.
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Journal of zoological systematics and evolutionary research
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10.1111/jzs.12278
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van Els, P., Norambuena, H. V., & Etienne, R. S. (2019). From pampa to puna: Biogeography and
diversification of a group of Neotropical obligate grassland birds (Anthus: Motacillidae). Journal of
zoological systematics and evolutionary research, 57(3), 485-496. https://doi.org/10.1111/jzs.12278
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J Zool Syst Evol Res. 2019;57:485–496. wileyonlinelibrary.com/journal/jzs
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4851 | INTRODUCTION
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 (e.g., Cuervo, 2013; Fernandes, Cohn- Haft, Hrbek, & Farias, 2015; Fjeldså, Bowie, & Rahbek, 2012; Harvey & 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, & Silva, 2003). For example, grassland taxa are presumably more vagile due to seasonal climatic fluctuations and
Accepted: 7 February 2019 DOI: 10.1111/jzs.12278
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 Els
1,2| Heraldo V. Norambuena
3,4| Rampal S. Etienne
11Groningen Institute for Evolutionary
Life Sciences, University of Groningen, Groningen, The Netherlands
2Department of Biological
Sciences, Museum of Natural
Science, Louisiana State University, Baton Rouge, LA
3Departamento de Zoología, Facultad de
Ciencias Naturales y Oceanográficas, Universidad de Concepción, Concepción, Chile
4Centro de Estudios Agrarios y Ambientales,
Valdivia, Chile
Correspondence
Paul van Els, Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The Netherlands. Email: paulvanels@gmail.com
Abstract
The 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 Haffer's 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 made.
© 2019 The Authors. Journal of Zoological Systematics and Evolutionary Research Published by Blackwell Verlag GmbH. Contributing authors: Heraldo V.
Norambuena (buteonis@gmail.com), Rampal S. Etienne (r.s.etienne@rug.nl)
fire regimes that force movements of grassland inhabitants (Hovick, Elmore, & Fuhlendorf, 2014; Little, Hockey, & 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 (“intermediate dispersal model,” Claramunt, Derryberry, Remsen, & Brumfield, 2012; Diamond, Gilpin, & Mayr, 1976; Phillimore, Freckleton, Orme, & 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 2,500 and 4,800 m (Román- 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 & Nyári, 2014). In addition, tropical grasslands are found in a ring around the Amazon Basin (“circum- Amazonian” dis-tribution, Remsen, Rocha, Schmitt, & 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 & 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 (Strömberg, 2011). There is some evidence that grassland- inhabiting organisms show an uptick in diversification during the development of grasslands (Agarwal & Ramakrishnan, 2017; Estep et al., 2014; Neiswenter & Riddle, 2010), mainly during the Miocene. Temporal estimates of the evolution of trop-ical C4 grasslands range from the early (Edwards, Osborne, Strömberg, & Smith, 2010; Strömberg, 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, & Fernandes- Filho, 2017; Burkart, 1975; Bush & Oliveira,
2006; Colinvaux, 1998; Patel, Weckstein, Patané, Bates, & 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, & Bastos, 2018; Van Els & Norambuena, 2018; Voelker, 1999a,b). 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 geogeo-graphic variation of diversification of grass-land birds across Neotropical open grass-landscapes.
Some species of Anthus are known for regular (Mild & Alström, 2010) and irregular long- distance movements (Brinkhuizen, Brinkhuizen, Keaveney, & Jane, 2010; Lees & 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 Anthus's spread to all major grassland areas on the South American continent across
time, to test the idea that the Andes were colonized multiple times from lowland grasslands.
2 | MATERIALS AND METHODS
2.1 | Samples and data collection
We obtained 39 tissue samples of all 22 subspecies- level taxa (Table 1) within the “New World Anthus clade” (Pietersen et al., 2018; Van Els & Norambuena, 2018; Voelker, 1999a); the remain-ing New World taxa belong to a mostly Asian clade. Most taxa are represented by >1 individual from localities as widely dispersed as possible within their ranges (Figure 1). Based on existing phylog-enies of Anthus, we chose A. cinnamomeus Rüppell, 1840 A. gustavi Swinhoe, 1863 A. rubescens, and A. rufulus Vieillot, 1818 as out-groups, because they represented closely related clades (Alström et al., 2015; Voelker, 1999a). We extracted total genomic DNA from pectoral muscle using a Qiagen DNeasy tissue extraction kit (QIAGEN, Valencia, California) following manufacturer's 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 2—ND2) and three nuclear genes: intron 2 of the myoglobin gene MYO (Heslewood, Elphinstone, Tidemann, & 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 8.1 (Kearse et al., 2012). We performed polymerase chain reactions (PCR) in 12.5 μl reactions using the following proto-col: denaturation at 94°C for 10 min, 40 cycles of 94°C for 30 s, vari-able annealing temperatures, and 72°C for 2 min, followed by 10 min elongation at 72 and 4°C 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 & Rakitov, 2008). We phased sequences in DnaSP using the algorithm provided by PHASE (Stephens & Donnelly, 2003), with an ambiguity cutoff of >0.7. 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).
2.2 | Phylogenetic analyses
We identified the best- fit nucleotide substitution model for each locus using jModeltest 2 (Darriba, Taboada, Doallo, & Posada, 2012; Guindon & 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. 2.3.2 (Drummond & Rambaut, 2007), achieving ESS values >200
for all parameter values. We used a calibrated Yule prior, and we ran the analysis for 100 million generations, sampling every 1,000. We analyzed posterior output in TRACER v. 1.5 and specified a burn- in of 10%. The mitochondrial ND2 locus was determined to evolve under a clocklike model in MEGA7.0 (Kumar, Nei, Dudley, & Tamura, 2008; AIC = 2,692.016). We used a lognormal substitution rate prior with a mean of 2.9 × 10−8 substitutions/site/year (Lerner,
Meyer, James, Hofreiter, & Fleischer, 2011) for ND2 and nuclear rates of 1.35 × 10−9 substitutions/site/year (Kimball et al., 2009),
applying lognormal distributions for most user- specified priors, except for base- frequency proportions (uniform) and population size priors (Jeffrey's). There are no fossil data from South America to describe the timing of diversification of the group, but a fossil Anthus from Pliocene deposits (4.3–4.8 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.
2.3 | Diversification analysis
To test for effects of diversity dependence across our tree, we used the R package DDD v. 3.5 (Etienne & 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, “shifting- rates model”). 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 5.3 Mya (Miocene–Pliocene boundary to test for effects of C4 grassland spread in South America), at 4.0 Mya (start of forma-tion of uppermost Andean vegetaforma-tion zones in older Central Andes, Pennington & Hughes, 2014), at 2.0 Mya (end of formation of upper-most Andean vegetation zones in young northern Andes, Pennington & Hughes, 2014), and at 1.8 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, Muñoz- Ramírez, & 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 birth–death model (function: bd_ML). For model comparison, we used AIC and the bootstrap likeli-hood ratio test of Etienne, Pigot, and Phillimore (2016) with 10,000 bootstrap replicates. We made a lineage- through- time plot of our data using the R package “paleotree.”
2.4 | Model- based biogeographic analysis
We used the dispersal- vicariance- like (DIVALIKE, Ronquist, 1997) and Bayesian analysis of biogeography when the number of areas
is large (BAYAREALIKE, Landis, Matzke, Moore, & Huelsenbeck, 2013) models in the package BioGeoBears (Matzke, 2012) imple-mented in R v.3.2.0. 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 dispersal–extinc-tion–cladogenesis model (Ree & 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. TA B L E 1 Taxon 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 Concepción; 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 – MF320010 MF320015 MF320056 MF320047
antarcticus BAS 3 South Georgia – MF320009 MF320016 MF320057 MF320048
bogotensis KUSNM 116,859 Ecuador Cotopaxi MF319979 MF320095 MF320070 MF320027
bogotensis LSUMZ 431 Peru Piura MF320026 MF320094 MF320069 MF320026
immaculatus KU 25,127 Peru Ayacucho MF320028 MF320105 MF320074 MF320028
meridae* AMNH 811,977 Venezuela Mérida MF320011 – – –
meridae* AMNH 811,978 Venezuela Mérida MF320012 – – –
shiptoni USNM 645,734 Argentina Tucumán MF320000 MF320111 MF320080 MF320034
shiptoni UWBM 54,394 Argentina Tucumán MF319999 MF320110 MF320079 MF320033
chacoensis* AMNH 797,085 Argentina Córdoba MF320008 – –
calcaratus LSUMZ 61,430 Peru Puno MF319985 MF320084 MF320051 MF320016
calcaratus LSUMZ 61,431 Peru Puno MF319986 MF320085 MF320052 MF320017
catamarcae UWBM 54511 Argentina Tucumán MF320001 MF320012 MF320081 MF320044
chilensis AMNH 13,589 Argentina Río Negro MF320035 MF320100 MF320060 MF320035
chilensis AMNH 13,591 Argentina Río Negro MF320036 MF320101 MF320061 MF320036
correndera USNM 630,116 Uruguay Tacuarembó MF319989 MF320088 MF320055 MF320020
grayi FIMNT Malvinas/
Falklands
– MF320007 MF320102 MF320071 MF320037
brevirostris KU 21,673 Peru Puno MF319996 MF320103 MF320072 MF320038
brevirostris KU 21,681 Peru Puno MF319997 MF320104 MF320073 MF320039
furcatus UWBM 54,556 Argentina Tucumán MF347705 MF320113 MF320082 MF320045
furcatus USNM 635,884 Uruguay Artigas MF320002 MF320114 MF320083 MF320046
brasilianus UWBM 54,574 Argentina Corrientes MF319991 MF320090 MF320059 MF320022
brasilianus USNM 630,210 Uruguay Tacuarembo MF319990 MF320089 MF320058 MF320021
dabbenei UCCC 2,376 Chile Araucania MF320013 MF320117 – MF320049
dabbenei UCCC 2,377 Chile Araucania MF320014 MF320118 – MF320050
hellmayri KU 9,813 Argentina Jujuy MF319994 MF320108 MF320077 MF320042
hellmayri UWBM 54,528 Argentina Tucumán MF319995 MF320109 MF320078 MF320043
abariensis USNM 626,029 Guyana Parabara MF319987 MF320086 MF320053 MF320018
abariensis YPM 13,701 Suriname Sipaliwini MF319988 MF320087 MF320054 MF320019
lutescens LSUMZ 87,109 Bolivia Santa Cruz MF320003 MF320098 MF320067 MF320029
lutescens USNM 645,602 Argentina Tucumán MF320004 MF320099 MF320068 MF320030
parvus LSUMZ 41,613 Panama Bocas del
Toro
MF319982 MF320093 MF320064 MF320025
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).
3 | RESULTS
3.1 | Phylogenetic relationships
ND2 was represented by 292/1041 variable sites, ACOI9 by 62/960, FIB5 by 37/581, and MYO by 34/723. 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. 2.3.2, 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 d'Orbigny 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.
3.2 | Timing and diversification
According to our BEAST v. 2.3.2 analysis, the ancestor of New World Anthus is estimated to have evolved ~7.5 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 ~5.8 Mya (Table 2) was the most likely model according to AICw,
and the second most likely model had a shift at ~1.8 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 = 0.05 (Figure 5).
3.3 | Biogeography
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 meridae/A. b. bogotensis/A. 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. furcatus/A. brevirostris) and two Andes- to- lowland dispersal events (A. hellmayri brasilianus/A. 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).
4 | DISCUSSION
4.1 | Miocene 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 5.8 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 44,804 Peru La Libertad MF319984 MF320097 MF320066 MF320032
peruvianus LSUMZ 48,218 Peru Lima MF319983 MF320096 MF320065 MF320031
nattereri KU 3,604 Paraguay Itapúa MF319992 MF320106 MF320075 MF320040
nattereri KU 3,665 Paraguay Itapúa MF319993 MF320107 MF320076 MF320041
spraguei LSUMZ 25,702 U.S.A. North
Dakota
MF319980 MF320091 MF320062 MF320023
spraguei LSUMZ 21,749 U.S.A. Louisiana MF319981 MF320092 MF320063 MF320024
cinnamomeus UWBM 5,2816 South Africa Eastern Cape AY329410 – – –
gustavi UWBM 75,556 Russia Primorsky
Krai HM538396 – – –
rubescens LSU 53,141 U.S.A. California MF320015 – – –
rufulus FMNH 358,350 Philippines Sibuyan KP671566 – – –
the relatively small number of tips in our tree. The shift in diversi-fication rates reflects the start of the diversidiversi-fication 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 (Strömberg, 2011). It is noteworthy that many other grassland- adapted taxa of South American origins such as Alectrurus and Muscisaxicola flycatchers (Fjeldså, Ohlson, Batalha- Filho, Ericson, & 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 “early burst” of diversification (Simpson, 1953) after its arrival to South America's 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 (Alström et al., 2015; Voelker, 1999a,b). 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. Many Mexican grasslands date from the Tertiary (Rzedọwski, 1975)
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 & Nyári, 2014) and Sturnella (Barker, Vandergon, & 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; Alström 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 (1999a,b). 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.
4.2 | The 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 ~1.7–1.8 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 I G U R E 1 Sampling 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
development of Andean habitats in relation to orogeny, it seems clear that large expanses of the highest vegetation zones probably developed during the last ~4.5 Mya of most intense orogeny (Hoorn et al., 2010; Madriñán, Cortés, & Richardson, 2013; Vuilleumier, 1969) and continue to the present (Madriñán 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 & Nyári, 2014), Muscisaxicola (flycatchers, Fjeldså et al., 2018), Hypericum (St. John's worts, Nürk, Scheriau, & Madriñán, 2013), and Lupinus (lupines, Hughes & Eastwood, 2006). The formation of Andean “islands” 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 & Simberloff, 1980).
F I G U R E 2 Biogeography 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. correndera/chilensis/grayi/antarcticus, and correndera Andes represents A. c. catamarcae/calcaratus. Tips may represent >1 individual, in which case they were collapsed. Pipit illustration Tyler, 2004
1.0 100% 0.98 97% 0.95 93% 0.93 93% 0.98 96% 0.91 85% 0.99 99% 0.99 100% 1.0 100% 1.0 100% 1.0 100% 1.0 100% 1.0 100% 0.97 97% 1.0 100% 1.0 100%
spraguei
brevirostris
furcatus
chacoensis
lutescens
parvus
brasilianus
hellmayri
meridae
correndera Andes*
correndera lowlands*
nattereri
peruvianus
bogotensis
shiptoni
immaculatus
dabbenei
F I G U R E 3 Biogeography 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
4.3 | Speciation 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 & 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 “cratonic” (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, & Cracraft, 2012) suggest-ing one of the many alternative theories explainsuggest-ing Amazonian spe-ciation (Arruda et al., 2017; Burkart, 1975; Bush & 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 I G U R E 4 Lineages- 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 Miocene/Pliocene 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
TA B L E 2 Output 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 −34.697 0.000 0.269 0.001 – – – DD 3 −31.504 0.021 2.047 0.324 16.577 – – SR 5 −28.377 0.065 1.157 0.001 8.999 19.489 1.682 SR5.8* 5 −25.874 0.791 9.542 0.344 1.273 16.386 5.856 SR5.3 4 −31.257 0.009 1.639 0.326 94.784 16.613 5.300 SR4.0 4 −31.381 0.009 2.211 0.301 13.855 16.516 4.000 SR2.0 4 −31.141 0.011 1.549 0.156 11.544 17.171 2.000 SR1.8 4 −29.021 0.092 1.097 0.001 8.999 19.641 1.800
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, & Moskovits, 1996; e.g., 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, & Lougheed, 2013), for which Pleistocene landscape pertur-bations may have driven rapid speciation in southern South American grasslands (Lijtmaer, Sharpe, Tubaro, & Lougheed, 2004). Regardless of the mechanism driving these diversity patterns, southern South America seems to be a center of diversification for Neotropical low-land grasslow-land birds.
4.4 | Short- 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 I G U R E 5 Bootstrap 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 = 0.05 with 10,000 replicates
TA B L E 3 Results 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 −LnL AICw d e DEC 2 30.724 0.001 0.032 0.035 DIVALIKE 2 25.942 0.008 0.031 0.000 BAYAREALIKE 2 38.794 0.001 0.033 0.222 DECc* 2 21.080 0.985 0.120 2.005 DIVALIKEc 2 25.942 0.008 0.030 0.000 BAYAREALIKEc 2 38.733 0.001 0.064 0.095
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 & 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 “j” pa-rameter in biogeographic models has been criticized recently (Ree & Sanmartín, 2018), because of the tendency of models includ-ing “j” 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 (e.g., HiSSE Beaulieu & O'Meara, 2016; SecSSE Herrera- Alsina, van Els, & Etienne, 2018). We consider sample size in our study to be insufficient for such relatively parameter- rich analyses.
ACKNOWLEDGMENTS
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 Fjeldså and Jan Bolding Kristensen (ZMUC), Jeremiah Trimble (MCZ), Kimball Garrett (LACM), Pablo Tubaro and Darío Lijtmaer (MACN), Alexandre Aleixo (MPEG), Jorge Pérez- Emán at the Instituto de Zoología Tropical at the Universidad Central de Venezuela, and Pedro Victoriano at the Universidad de Concepción in Chile. Andy Wood at the British Antarctic Survey provided valua-ble samples of A. c. antarcticus. Sabrina Taylor at LSU's 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 P.A. Hens Memorial Fund, an American Ornithologists’ 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- PCHA/DoctoradoNacional/2013- 21130354 schol-arship. RSE thanks the Netherlands Organization for Scientific Research (NWO) for financial support through a VICI grant. ORCID
Paul van Els https://orcid.org/0000-0002-9499-8873
Heraldo V. Norambuena https://orcid.org/0000-0003-0523-3682
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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. 2019;57:485–496.
