A behavioral polymorphism as an intermediate stage in the evolution of divergent forms - partial migration in New World Flycatchers (Aves, Tyrannidae)

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A behavioral polymorphism as an intermediate stage in the evolution of

divergent forms: partial migration in New World Flycatchers (Aves,

Tyrannidae)

By Valentina Gómez Bahamón

Thesis submitted in partial fullfillment of the requirements for the degree of Master of

Science

Advisor:

Daniel Cadena Ph.D.

Departamento de Ciencias Biológicas

Universidad de los Andes

Departamento de Ciencias Biológicas

Facultad de Ciencias

Universidad de los Andes

Colombia

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Some of the analyses of this project were completed in collaboration with Roberto

Marquez

1

_{and Oscar Laverde}

2

_.

1

_{Department of Ecology and Evolution, University of Chicago – USA}

2

_{Laboratorio de Biología Evolutiva de Vertebrados, Universidad de Los Andes, Bogotá –}

Colombia

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Acknowledgements:

For insightful comments on the manuscript we thank Fransisco Pulido and Adolfo

Amézquita. For valuable comments we thank Nick Bayly, Chris Witt, Trevor Price, Ben

Winger, Fabrice Schmitt, and Alex Jahn. For statistical advice we thank Liam Revell and

Daniel Moen. This project was funded by a "Proyecto Semilla" of the Facultad de

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Abstract

Migratory behavior is a complex trait found in many animal groups. In birds, migration

has been found to be a highly labile trait that has evolved repeatedly in different lineages.

The evolution of migration evolves in birds has been the subject of multiple studies

assessing the ecological factors that promote its origin, the hereditary basis of the traits

associated to it, its geographic origin and its association with species diversification.

Partial migration is a strategy in which some individuals of a population or a species

migrate and others stay as permanent residents. Few studies have examined the

evolutionary origin of partial migration from a macroevolutionary perspective and none

has assessed the role that it can play in species diversification. In this study we explicitly

tested whether partial migration is an intermediate step in the evolution of full migration

and sedentariness in a large family of birds, the New World Flycatchers (Aves,

Tyrannidae). We tested different models of trait evolution allowing and disallowing

transitions among character states and found that, not only is partial migration an

intermediate step in between migration and sedentariness, but also that the loss of

migration is more common than its gain. These findings suggest that more attention

should be devoted to understanding the forces leading to the loss of this behavioral trait.

We also tested speciation and extinction models associated to partial migration, finding

evidence that partial migration is associated with high speciation rates in the Tyrannidae.

Finally, we tested if there where differences in the number of partially migratory lineages

and fully migratory lineages associated to current geographic distribution and ecological

context, finding that there are significantly more partial migrants in the southern

hemisphere and more fully migratory species in the northern hemisphere. Thus, studies

on the evolution of migration should involve comparisons between migratory systems

allowing for a better understanding of the factors that promote its evolution. Our findings

highlight the importance of understanding partial migration at a macroevolutionary scale

to better understand the evolution of migration.

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“Now, before our very eyes as it were, a development ocurred that turned this partial

migrant into a migrant. The partial migrant, which in autumn originally wandered off in

all directions from its breeding grounds, when it breeds further north becomes a partial

migrant that predominantly turns southward, and at our latitude finally becomes a true

migratory bird…It is very remarkable that the migratory drive gradually became

stronger and stronger… Has the migratory drive become stronger by elimination of

individuals with a weak drive (selection)…?... I shall leave it to evolutionary

theoreticians to draw conclusions from this behavior of the Serin! The only thing certain

is the fact that the migratory drive has intensified.”

Ernst Mayr 1926, translated in Berthold 1999.

Introduction

Every year, massive movements of animals occur in response to variation in

seasonal environments (Dingle 1996, Alestam et al 2003, Newton 2008). Migratory

behavior has evolved in several invertebrate and vertebrate species (Dingle 1996), and is

ubiquitous among animals. In birds, migratory behavior is a highly labile trait, which has

evolved repeatedly in many different lineages (Helbig 2003). The evolution of migratory

behavior in birds has been the subject of many studies, with some assessing the

ecological factors that promote its origin (e.g. Cox 1985, Levey & Stiles 1992, Boyle &

Conway 2007, Shaw & Couzin 2013), others examining the hereditary basis of traits

associated with migratory behavior (e.g. Berthold 1988, Helbig 1991, Berthold et al

1996), and others testing hypotheses about the geographic origins of migration (e.g.

Cooke 1915, Rappole 1995, Helbig 2003, Salewski & Bruderer 2007, Winger et al.

2014). In addition, a few recent studies have examined the evolutionary consequences of

migration from a macroevolutionary perspective, finding that migratory behavior may

promote speciation and drive lineage diversification (Winker 2010, Rolland et al. 2014).

A prominent hypothesis proposed to explain the evolution of migratory behavior

posits that migration evolves in a stepwise process, involving transitional stages between

sedentariness and full migration (Cox 1985, Bell 2000). This “stepping-stones

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distribution ranges during the breeding period towards temperate seasonal environments

in response to selective pressures involving factors such as climate, resource availability,

and biotic interactions (e.g., competition, predation, parasitism). If moving to seasonal

environments during the breeding season represents fitness rewards exceeding the costs

of migrating, then differentiation from sedentary populations could occur (Cox 1985, Bell

2000). An ancillary hypothesis posits that all birds have the potential to evolve migratory

behavior in the form of standing genetic variation and that, given this predisposition,

migration will readily evolve once selective pressures favoring this behavior arise;

conversely, migration can be easily lost given external pressures (Berthold 1999). This

appears plausible because many traits associated with migratory behavior seem to evolve

as a syndrome (i.e., as a suite of correlated traits) involving joint modifications in life

histories, morphology and physiology (Dingle 1986, Faibairn 1994).

Partial migration is a common phenomenon among birds where some individuals

of a population or species migrate and others stay as permanent residents (Rappole 1995,

Dingle 1996, Pulido 2007, Newton 2008). How partial migration evolves and the factors

that promote its evolution have been the focus of several theoretical studies (Cohen 1967,

Cox 1985, Lundberg 1987, Kaitala et al. 1993, Chan 2005, Taylor and Norris 2007, Shaw

and Levin 2011, Pulido 2011), as well as of microevolutionary experimental work

(Pulido et al. 1996, Pulido & Berthold 2010). However, at a macroevolutionary scale,

little is known about the role that partial migration plays in the evolution of migratory

lineages. Studies examining the phylogenetic evidence for partial migration being an

intermediate step between sedentariness and full migration are scarce and their results are

mixed (Kondo and Omland 2007, Amaral et al. 2009). In addition, studies on the topic

have relied on reconstruction of ancestral character states, which are highly uncertain due

to the lability of migratory behavior (Blomberg et al. 2003), and have focused on groups

having too few species to draw any inferences about general patterns in the evolution of

migration with statistical power. Thus, to our knowledge, the hypothesis that partial

migration represents an intermediate stage in the evolution of fully migratory and resident

lineages has not been explicitly tested in a macroevolutionary framework in a large clade

exhibiting ample variation in migratory behavior. Likewise, the role that partial migration

plays in lineage diversification remains unstudied.

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A long-standing, commonly accepted assertion is that migratory species evolved

from tropical sedentary species (Helbig 2003). However, recent evidence suggests this

scenario may need reevaluation because it does not apply to all cases (Winger et al. 2012,

Voelker et al. 2013). For example, it was recently shown that in emberizoid passerine

birds (arguably the largest radiation involving migrant landbirds in the New World),

migratory behavior evolved primarily through shifts in winter ranges to tropical areas

from North American ancestral ranges (Winger et al. 2014). Another recent study

provided evidence that migratory lineages commonly diversify into one sedentary lineage

that “settles down” (i.e., loses migration) and another lineage that retains migration

(Rolland et al. 2014). This results in higher net diversification rates in migratory lineages

than in sedentary lineages even though the latter are more numerous.

Although much has been learned about the origin of migratory lineages and of the

evolutionary consequences of migration from recent comparative analyses in a

phylogenetic framework, studies on the topic have typically not considered partial

migration as a character state different from full migration. Because partial migration has

been hypothesized to be an intermediate stage between sedentariness and full migration,

treating partial migration and full migration in a single category could limit one's ability

to uncover evolutionary processes relevant to understanding the origin of migratory

behavior and its role in species diversification. In particular, by treating partial migrants

and full migrants equally, earlier studies have been unable to assess the role that partial

migration may play in the diversification of avian lineages.

Most studies on the evolution of migration have been conducted on boreal

migrants that breed in the northern temperate zone and migrate to tropical areas during

the non-breeding period (Newton 2008, Pulido 2007). This limits the range of ecological

conditions that have been considered in evolutionary studies of migration (Pulido 2007).

Birds that reproduce in the southern temperate zone also migrate in response to seasonal

fluctuations (i.e. austral migrants), including species from Africa, Australia and South

America (Zimmer 1938). In South America, little is known about the mechanisms that

promote the evolution of migration in austral lineages, which may differ from the

mechanisms operating in the Northern Hemisphere (Jahn et al. 2010). A study that

evaluated the factors that promote the evolution of austral migration in a phylogenetic

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comparative framework found a correlation between habitat type and the evolution of

migratory behavior (Chesser & Levey 1998). These results contrast with those of a study

in the Motacillidae family from the Northern Hemisphere, in which there was no

correlation between migration and habitat type (Outlaw & Voelker 2006). This

discrepancy may partly reflect that the selective pressures faced by austral migrants may

differ from those faced by boreal migrants. For instance, due to geographic features of the

American continent, patterns of spatial variation in climatic conditions differ between

hemispheres, with temperature changing more strongly with latitude in North America

(Petitpierre et al 2012). Moreover, the conditions that birds encounter along their

migratory routes likely differ between hemispheres as well. Species breeding in North

America need to either cross the Gulf of Mexico to get to South America or travel

through Central America to reach their wintering grounds (Zimmer 1938, Chesser 1994).

Those crossing the Gulf of Mexico must fly over the Caribbean Sea, requiring

adaptations to help them fuel extensive flights (Bayly et al. 2013), whereas those

migrating through Central America are funneled through the geographic narrowing of the

continent, where available territories are likely limited. In contrast, South American birds

that migrate northward into the tropics face an increasingly wide geographic area

(Zimmer 1938, Chesser 1994).

Large ecological barriers such as oceans and deserts may constrain the evolution

of migratory strategies preventing shifts in breeding and wintering ranges (Henningsson

& Alestam 2005). Most austral migrants involve partial overlap of breeding and

wintering ranges, and migratory distances tend to be shorter than in boreal migrants,

probably as a result of the South American geography (Chesser 1994). Due to the above

differences in climatic factors, flying distances and ecological barriers experienced by

migrants, one may hypothesize that selective pressures to evolve full migration would be

stronger in North temperate zones than in South temperate zones. This hypothesis

predicts that one would find more fully migratory lineages breeding in the temperate zone

of North America than in the temperate zone of South America, where partial overlap of

breeding and wintering ranges can occur (Chesser 1994).

The New World flycatchers (Tyrannidae) represent the largest family of birds in

the Western Hemisphere, with approximately 100 genera and 430 species (Rheindt et al.

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2007). Because the family includes multiple resident, migratory and partially migratory

lineages, it represents an ideal model in which to test hypotheses about the role of partial

migration in the evolution of migratory behavior and its macroevolutionary

consequences. In addition, because the Tyrannidae includes several lineages of boreal

migrants and many austral migrants, one may use them to examine geographic patterns of

variation in migratory behavior.

In this study, we tested hypotheses about the role that partial migration plays in

the evolution of migratory behavior in the Tyrannidae using a comparative phylogenetic

approach. We reconstructed ancestral character states to determine the frequency and

direction of transitions between partial migration, full migration and sedentariness in the

Tyrannidae, and tested models of character evolution to determine whether partial

migration represents an intermediate evolutionary stage linking full migration and

sedentariness. We also examined the evolutionary consequences of migration and partial

migration by assessing the relationship between diversification rates and migratory status.

Finally, we examined whether there is an association between migratory system (i.e.,

boreal, austral) and the evolution of fully migratory lineages and partially migratory

lineages. Our analyses reveal that considering partial migration is crucial to better

understand the evolution of migratory behavior and the links between microevolutionary

and macroevolutionary processes associated with the origin of migratory behavior.

Methods

Phylogenetic inference.

Phylogenetic studies on the Tyrannidae and other groups

have generated sequence data for members of the family, but a comprehensive

phylogenetic hypothesis for the group is lacking. We thus compiled published data

available in GenBank (downloaded using PhyLoTa Browser; Sanderson et al. 2008) and

used them to reconstruct a phylogeny based on sequences of two mitochondrial genes and

six nuclear loci totaling 8,518 base pairs for 329 species in the Tyrannidae, comprising

77% of the total number of species in the family (Table 1). We adopted a ‘supermatrix’

approach, which consists of combining all characters (in this case sequences of all eight

genes) into a single phylogenetic matrix and then analyzing all character data

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sequences for all the genes, our supermatrix had a total of 59.4% missing bases; on

average, each species included in the analyses had data for 3,536 base pairs (41.6%;

range 284-8507 bp [3%- 100%]). We chose to include species with large fractions of

missing data to allow for more comprehensive comparative analyses; we believe this is

justifiable because adding characters with missing data often improves accuracy in

phylogeny estimation (Wiens & Morrill 2011). When more than one sequence was

available for a given species, we aligned them in the software Geneious (Drummond et

al. 2011) and obtained a consensus, resulting in a single sequence per species in our final

alignment. We tested the best-fit model of sequence evolution for each gene in

PartitionFinder (Lanfear et al. 2012) for coding sequences and in Modeltest (Posada &

Crandall 1998) for non-coding sequences (i.e., introns). The resulting supermatrix was

used to estimate the posterior distribution of phylogenetic trees under a Bayesian

framework in the program BEAST (Drummond et al. 2012). We performed four separate

runs, each for 50,000,000 generations, sampling every 5,000 generations implementing a

relaxed molecular clock. Chains were visually inspected in Tracer (Rambaut et al. 2014)

to determine the burnin value which was 15,000,000 in 3 of the runs and 20,000,000 in

the other run (resulting in a post-burnin of 135,000,000 generations). A Yule process for

speciation was used and priors were set using default values, except for clock rates for

which we used a uniform prior with rates between 0 and 20. Finally, to obtain a single

maximum clade-credibility tree, we combined the entire posterior distribution of 20,000

trees using LogCombiner in BEAST.

Character-state classification.

We defined migratory birds as those that move

annually to overwinter in a different location after reproduction and then return to the

same location continuing on a yearly cycle. Partial migrants are species in which one

subspecies or population is migratory and another subspecies or population is sedentary.

This category includes cases in which migratory and resident populations breed in the

same geographic region, as well as those in which they reproduce in different regions,

although the former situation is rare. Sedentary lineages are those that stay year-round

within a relatively small geographic range and show no evidence of cyclical movements.

Based on published data (Del Hoyo et al. 2004), we assigned character states (migratory,

partial migrant, sedentary) to every species of Tyrannidae in our phylogeny. We focused

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only on latitudinal migration (i.e. boreal or austral migration) and did not consider

altitudinal migration. We also classified migratory and partially migratory species as

boreal or austral migrants. We defined boreal lineages as those having at least one

migratory population breeeding in areas north of the Tropic of Cancer (23.5ºN) and

austral lineages as those having at least one migratory population breeding in areas south

of the Tropic of Capricorn (23.5ºS).

Is partial migration an intermediate step in the evolution of full migration?

To

determine whether partial migration is and intermediate step in the evolution between

migratoriness and sedentariness in the Tyrannidae, we reconstructed and mapped

ancestral character states on the phylogeny and tested different models of trait evolution.

We examined trait evolution using two kinds of comparative phylogenetic models to

ensure that our results were robust to different statistical assumptions. First, we used a

model in which character states change under a continuous-time discrete-state Markov

process (Pagel 1994 & Pagel 1999), where the probability of changing between states

does not depend on prior states (hereafter

Mk

-model). Second, we used a threshold model

adopted from quantitative genetics in which character states change gradually depending

on a continuous trait (Felsenstein 2005, Felsenstein 2012, Revell 2014). The threshold

model was proposed to describe the evolution of discrete character states with a

polygenic basis (Wright 1934). In theory, for certain discrete characters, every individual

in a population has a value for a continuous character (i.e., the "liability") determined by

the polygenic genotype and the environment. However, the phenotypic expression of this

character is not continuous; rather, it is expressed discretely depending on a threshold

value of the liability (Wright 1934, Felsenstein 2005, Felsenstein 2012, Revell 2014).

Mk

model

.

To determine whether a model with partial migration as an

intermediate state between sedentariness and migratoriness is supported in the

Tyrannidae, we tested all possible models of character-state transition across the

complete posterior distribution of 20,000 trees (i.e including models with all the possible

transitions among the three character-states). Models were run allowing and disallowing

transitions (Table 1) in the R package

diversitree

(FitzJohn 2012). Akaike information

criterion weights (AICw) and Bayesian information criterion weights (BICw) were

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can change instantly with an equal probability of reversal (Revell 2014), which might be

unrealistic for complex traits such as migration. However, an advantage of using

Mk

models is that they allow one to estimate transition rates between character states based

on ancestral state reconstructions.

Threshold model. The threshold model has recently been implemented into

comparative phylogenetic analyses allowing reconstruction of ancestral character states

and the examination of trait evolution (Felsenstein 2005, Felsenstein 2012, Revell 2014).

Because it incorporates a plausible biological model of phenotypic evolution in

comparative phylogenetic analyses, the threshold-model approach is likely more

biologically realistic than the approach based on

Mk

models. However, transition rates

between character states cannot be estimated under existing implementations of the

threshold model.

To determine whether partial migration is an intermediate step between

migratoriness and sedentariness assuming the threshold model, we tested all possible

transition sequences under a Brownian-motion model of trait evolution in the R

package

phytools

using Markov Chain Monte Carlo sampling (Revell 2012). There are

three possible sequences by which transitions can occur: (1) from migratory to partially

migratory to sedentary (M

↔

P

↔

S), (2) from partially migratory to sedentary to

migratory (P

↔

S

↔

M), and (3) from partially migratory to migratory to sedentary

(P

↔

M

↔

S). We estimated the effective sample size of parameters in the R

package

coda

(Plummer, 2006) and visually inspected chains to assess proper mixing and

determine the burnin in Tracer. We tested the three models of trait transition-sequence for

10,000,000 generations with a burnin of 1,000,000 generations. Model statistical support

was assessed using Deviance Information Criterion (DIC) values estimated

in

phytools

and DIC weights calculated in the R package

paleoTS

.

Do diversification and extinction rates vary in association with migratory

strategy?

To test for associations between migratory strategy and evolutionary

diversification in the Tyrannidae, we tested Multi-state Speciation and Extinction models

(

MuSSE

) in the R package

diversitree

(FitzJohn 2012). This method analyzes the

evolution of traits with multiple character states and estimates speciation (

λ

) and

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following a continuous-time discrete-state Markov process along the branches of a tree

(FitzJohn 2012).

We first examined statistical support for various models describing diversification

and extinction rates in 2,000 trees in the posterior distribution based on AICw and BICw

values. The models tested consisted of: (1) allowing all diversification rates and

extinction rates associated to a character state to be different, (2) constraining

diversification rates and extinction rates associated to a character state to be equal, (3)

constraining diversification rates associated to a character state to be equal and allowing

extinction rates to differ, and (4) allowing diversification rates associated to a character

state to differ and constraining extinction rates associated to a character state to be equal.

We selected the model with highest support as the basis to estimate diversification and

extinction rates associated to each character state.

Is there an association between migratory system (austral/boreal) and migratory

strategy (partially/fully migratory)

? To assess whether partial migration and full

migration evolve in relation to geographic area (austral or boreal), we implemented a

statistical method that examines the correlation between discrete characters taking into

account phylogenetic history, branch lengths, and rates of character-state change (Pagel

1994). Two models are tested under this method: (1) allowing for correlated evolution of

the two characters, and (2) assuming independent evolution of the two characters. To

determine statistical support, we implemented a likelihood-ratio

χ

2

approach (4 degrees

of freedom) and also calculated 1,000 simulations in Mesquite to compute a

p

-value for

significance (Maddison & Maddison 2014). Because our question pertained only to

migratory species, we pruned the phylogeny to include only species that are either

migratory or partially migratory, and that are boreal or austral. Including sedentary

species would bias our analyses because the vast majority are tropical. Thus, including

residents one would find a relationship between behavioral strategy and geography

without obtaining information about the question regarding migratory strategy. A total of

90 species were used in the analysis. Because the analysis of evolutionary correlation

between discrete traits that we used has only been implemented for binary traits, species

having both boreal- and austral-breeding populations were excluded from the analysis (6

out of 96 migratory lineages were excluded).

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Results

We classified 70.5% of the 329 species of Tyrannidae as sedentary, 20.1% as

partially migratory, and 9.4% as migratory. Estimated ancestral character states differed

somewhat between the

Mk

model and the threshold model of trait evolution (figures 1A

and 2). Overall, the

Mk

model reconstructed ancestral character states with more

uncertainty than the threshold

model. In

Mk

models many ancestral states were

reconstructed as fully migratory, whereas under the threshold model partial migration and

sedentariness were the dominant ancestral character states. The ancestor of the family

was reconstructed as uncertain in the

Mk

model, but it was reconstructed as sedentary

with a high probability under the threshold model. Throughout the phylogeny, both

models reveal gains and losses of migratory behavior, but loss of migratory behavior

seems to have been more common.

Is partial migration an intermediate step in the evolution of full migration?

Analyses of trait evolution strongly supported the hypothesis that partial migration is an

intermediate step in between sedentariness and full migration.

Mk

models with the

highest support were those disallowing direct transitions from a migratory to a sedentary

state and vice versa (figure 3). Likewise, under the threshold-model approach, the model

with highest support corresponded to the evolutionary sequence of trait transition from a

migratory to a partially migratory to a sedentary character state (M

↔

P

↔

S; table 2).

Rates of transitions between character states were estimated under the

Mk

model.

The path with higher transition rates was that from a partially migratory to a sedentary

state (median transition rate= 52.6), followed by changes from a migratory to a partially

migratory state (median transition rate = 30; Figure 1B). Transition rates from a sedentary

to a partially migratory state and from a partially migratory to a migratory state were

lower (median transition rate of 9.8 and 7.2, respectively); the rate of change between

migratory and sedentary states was ~0 (Figure 1B).

Do diversification and extinction rates vary in association with migratory

strategy?

The model with highest support was one with where diversification rates

differed with respect to character state (i.e., migration, partial migration and

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model, diversification rates were higher in migratory lineages (median=38.18, highest

posterior density 97.5%=44.450, 2.5%=33.989), followed by partially migratory lineages

(median=31.41, highest posterior density 97.5%=37.382, 2.5%=25.662), and by

sedentary lineages (median=14.34, highest posterior density 97.5%= 15.867, 2.5%=

9.631; figure 4B). Because extinction rates were estimated to be ~0, net diversification

rate was equal to the speciation rate.

Is there an association between migratory system (austral/boreal) and migratory

strategy (partially/fully migratory)

? We found that migratory strategy (i.e. partial

migration or migration) was strongly associated with migratory system (austral or

boreal). Partial migrants occur significantly more frequently in the austral migration

system, whereas full migrants are more commonly found among boreal migrants (figure

5). The difference in likelihood (DLnL=8.7795) between the two models (i.e. correlation

between migratory system and geographic area and no correlation) was significant based

on the

χ

2

approach (likelihood ratio= 2*DLnL=17.559, p=0.0015) and also based on the

simulation approach (p<0.001, 1000 simulations).

Discussion

We assessed the role that partial migration plays in the evolution of full migration

and its macroevolutionary consequences in the avian family Tyrannidae. We found strong

support for partial migration being an intermediate step linking the evolution of full

migration and sedentariness, and that migratory and partially migratory lineages exhibit

significantly higher diversification rates than sedentary lineages. We also found that fully

migratory species are significantly more numerous among boreal migrants whereas

partially migratory species are significantly more numerous among austral migrants,

suggesting that the conditions promoting the evolution of different types of migratory

behavior differ between the Northern and the Southern hemispheres of the New World.

In the Tyrannidae, migratory behavior has evolved independently multiple times,

supporting the idea that migration is an evolutionary labile trait (Helbig 2003). Our

analyses reveal that loss of migration was more common than its gain. This is evidenced

by the reconstruction of ancestral character states on the phylogeny and by higher

transition rates occurring from migratory states passing through partial migration to

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sedentary states than the other way around. Our results contradict the assertions that

migratory species evolved from tropical sedentary species and that the gain of migratory

behavior occurs much more often than its loss (Helbig 2003). This finding is in

agreement with other macroevolutionary studies that have found that sedentary species

often evolve from migratory ancestors in birds (Winger et al. 2012, Voelker et al. 2013,

Rolland et al. 2014) and other organisms (Zhan et al. 2014). This finding is also in

agreement with previous evidence that the gain of migratory behavior is rare in

comparison to the loss of migration (Berthold 1999). Many examples from different

species have been reported of individuals reducing migratory activity and forming

sedentary populations (Berthold 1998), but examples of individuals gaining migration are

scarce (e.g., Able & Belthoff 1998). It is still not clear if this pattern occurs because

gaining migration is less probable because there are many adaptation that would have to

evolve for migration to be possible, or because the current, relatively warm, interglacial,

climatic conditions (Tzedakis et al. 2009) favor the loss of migration (Zink 2011).

At a macroevolutionary scale, little is known about the role that partial migration

plays in the evolution of migratory lineages. We explicitly tested hypotheses of trait

evolution in the Tyrannidae and found that partial migration is in fact an intermediate

step linking the evolution of migratory behavior and sedentariness, suggesting that

microevolutionary (i.e., population-level) patterns in which partial migration is an

intermediate step between migratoriness and sedentarism (Berthold 1999) also hold at a

macroevolutionary scale (see also Amaral et al. 2009). The “stepping-stones hypothesis”

postulates that a population of tropical sedentary species may expand its distribution

rangs during the breeding period towards temperate seasonal environments in response to

selective pressures involving an intermediate stage of partial migration (Cox 1985). Our

results partially support this hypothesis because direct transitions from sedentary to fully

migratory states in the Tyrannidae were extremely rare, and transitions between these

states involving partial migration were more frequent. However, the most important and

novel insight provided by our analyses of trait evolution is that partial migration is most

frequently a crucial intermediate step in the evolutionary loss of migration. Taken

together, our results and those of several recent studies revealing the high frequency with

which migration has been lost, suggest that considerably more attention should be

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devoted to understanding the forces leading to the loss of migration, as most of the

literature seeking to account for differences in migratory behavior among lineages has

focused on the gain of migration.

The existence of an intermediate stage like partial migration facilitates the

occurrence of shifts between sedentarism and migratoriness (Berthold 1999). Birds that

migrate require complex physiological and morphological adaptations allowing them to

accomplish long flights at a precise timing and in accurate directions towards locations

that are often ecologically very different (e.g. Berthold 2001, Zink 2002, Alestam et al.

2003). It appears puzzling, then, that such a complex behavioral trait may be highly labile

evolutionarily (Helbig 2003) and may be gained or lost over a small number of

generations (Pulido & Berthold 2010). However, genetic correlations exist among

life-history, morphological and physiological traits associated with migratory behavior

(Dingle 1986, Fairbairn 1994, Dingle 1996), and such correlations result in multiple

phenotypic traits being jointly affected by selection (Pulido 2007).

We found that in the Tyrannidae, speciation rates differ among migratory,

partially migratory, and sedentary lineages. Although much has been learned about the

origin of migratory lineages and of the evolutionary consequences of migration from

recent comparative analyses in a phylogenetic framework, studies on the topic have

typically not considered partial migration as a character state different from full migration

(e.g., Rolland et al. 2014). Our results show that treating partial migration and full

migration in a single category could limit one's ability to uncover its role in species

diversification. We found that speciation rates were higher in migratory lineages, but

were also high in partial migrants. Had we treated partial migrants and full migrants

equally we might have incorrectly estimated the effect of migration and would have

ignored an important character state (i.e., partial migration) that could also potentially be

promoting speciation.

Migratory behavior has been proposed to result from differential use of resource

peaks occurring in allopatric locations (Winker 2010). If different resource peaks in

allopatry are exploited during the breeding season, then this may result in reproductive

isolation, a process termed heteropatric speciation (Winker 2010). Although little is

known about the role of behavior in species divergence, behavioral polymorphisms such

(18)

as partial migration may result in ecological differentiation and evolutionary divergence

(Smith & Skulason 1996). Based on the above theoretical work and our results, we

suggest that future studies should consider partial migration as a trait potentially

promoting speciation and should examine its influence separately from that of full

migration.

Selection pressures promoting the evolution of full migration may differ among

North temperate birds and South temperate birds; such pressures involve factors like

climate, the shape of continents, flying distances, and major ecological barriers faced by

migrants (Zimmer 1938, Chesser 1994). We found that there are significantly more fully

migratory species breeding in the temperate zone of North America than in the temperate

zone of South America, and that there are significantly more partially migratory species

breeding in the temperate zone of South America than in the temperate zone of North

America. These results are consistent with the hypothesis that selection pressures

promoting the evolution of full migration are stronger in the Northern hemisphere than in

the temperate zone of South America, where partial overlap of breeding and wintering

ranges can occur due to continental shape (Chesser 1994). Most studies assessing the

ecological factors that promote migratory behavior have focused on either migratory

system, but have not considered that conditions might differ and this may explain

contrasting results in different studies (e.g. Chesser & Levey 1998 in the austral system

vs. Outlaw & Voelker 2006 in the boreal system). We suggest that additional work

involving comparisons between migratory systems would allow for a better

understanding of the role of partial migration in the evolution of migration, and more

generally, of the factors that promote migratory behavior.

A potential caveat of our study is that we treated partial migration as a single

character state, but in fact partial migration is a strategy found in a variety of forms,

which are likely not homologous to each other (Zink 2011): (1) migrants and residents

can breed in sympatry but overwinter apart, (2) migrants and residents can overwinter

together and breed in allopatry, (3) and individuals can migrate to breed elsewhere but

not every year (Chapman et al 2011). Moreover, partial migration is fixed in some

species (i.e. migrants move every year and residents stay permanently), whereas in a few

species it occurs facultatively (Chan 2005). These different kinds of partial migration

(19)

arguably represent stages in a continuum (Berthold 1999), just as partial migration is

intermediate in between sedentariness and full migration. We suggest that examining the

evolution of different kinds of partial migration separately in future studies may enhance

our ability to uncover evolutionary patterns and to identify the ecological drivers of

evolutionary processes relevant to understanding the origin of migratory behavior (Zink

2011).

Partial migration is widespread in the animal kingdom (Chapman 2011) and has

been suggested to play an important role in the evolutionary processes shaping migratory

behavior. Here we demonstrate that considering partial migration in macroevolutionary

studies is crucial to further understand the evolution of migratory behavior and its role in

speciation. Not only did we show that partial migration represents an intermediate

evolutionary stage between two different life-history strategies (i.e, migratory behavior

and sedentariness), but we also demonstrated that partial migration is associated with

high speciation rates. Moreover, our finding that there are different patterns in species

being partially migratory or fully migratory between the northern and southern

hemisphere suggest that migratory systems evolve under different selective pressures, a

pattern worth considering before drawing conclusions about the factors that promote

migratory behavior. Comparing factors such as climate, resource availability, and biotic

interactions (e.g., competition, predation, parasitism) among migratory systems is crucial

to further understanding how migratory behavior evolves, a question that has fascinated

scientists and natural historians for over two millennia (Chapman et al. 2011).

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Figure legends:

FIGURE 1A

Full migration and partial migration have evolved multiple times over the

phylogenetic history of the Tyrannidae. Ancestral character states show that partial

migration is often an intermediate step between full migration and sedentariness,

although in many cases ancestral states are reconstructed with uncertainty. The

phylogenetic reconstruction was done with 2 mitocondrial genes and 6 nuclear genes

sampled for 329 species. Character states and ancestral reconstructions are mapped using

the

Mk

model. White represents sedentary lineages, red partial migrants, and black full

migrants.

FIGURE 1B

Partial migration is an intermediate step in the evolution between full

migration and sedentariness in the Tyrannidae. Loss of migration has occured more often

than its gain.

Median transition rates are calculated using the

Mk

model in the 20,000

trees of the posterior distribution, allowing all possible transitions to occur. Arrow width

is proportional to the value of the transition rate. Arrows indicate the direction in which

the transition of character state occurs.

FIGURE 2

Full migration and partial migration have evolved multiple times over the

phylogenetic history of the Tyrannidae. Ancestral character states are reconstructed with

certainty and partial migration is often an intermediate step between sedentariness and

full migration. The phylogenetic reconstruction was done with 2 mitocondrial genes and

6 nuclear genes sampled for 329 species. Character states and ancestral reconstructions

are mapped using the threshold model under Brownian motion. White represents

sedentary lineages, red partial migrants, and black full migrants.

FIGURE 3

Partial migration is an intermediate step in the evolution between sedentary

and migratory species.

Support for the 10

Mk

models testing character-state transitions by

constraining and allowing all combinations of transitions show that the model with

highest support corresponds to partial migration as an obligatory intermediate step. To

account for phylogenetic uncertainty, all models were tested in the complete posterior

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distribution of 20,000 trees. Support was calculated based on AICw and BICw. Dots

represent the median and credibility intervals correspond to highest posterior density

(HPD). Model 1 has no restrictions and Model 2 corresponds to the hypothesis of partial

migration as an intermediate step in the evolution of full migration from sedentariness

and vice versa.

FIGURE 4A

In the Tyrannidae, speciation rates differ in association with behavioral

strategy (i.e., migration, partial migration and sedentariness), but extinction rates show no

association with these character states.

This is evidenced by the support for the

5 MuSSE

models tested for diversification (

λ

) and extinction (

µ

) rates. To account for

phylogenetic uncertainty, all models were tested in 2,000 trees selected randomly from

the posterior distribution. Support was calculated based on AICw and BICw, dots

represent the median, and credibility intervals correspond to the highest posterior density

(HPD).

FIGURE 4B

Speciation rates are significantly higher in association to both migration

and partial migration, relative to to sedentariness. Estimated diversification rates were

calculated using the

MuSSE

model allowing all parameters to vary. The estimated values

of diversification rates associated to sedentarism are between 9.631 (2.5%) and 15.867

(97.5%), to partial migration are between 25.662 (2.5%) and 37.382 (97.5%), and to

migration are between 33.989 (2.5%) and 44.450 (97.5%). To account for phylogenetic

uncertainty, all models were tested in 2,000 trees selected randomly from the posterior

distribution.

FIGURE 5

There are more partially migratory species in the southern hemisphere than in

the northern hemisphere of the Americas and there are more fully migratory lineages in

the northern hemisphere than on the southern hemisphere.

Results indicate a significant

relationship between migratory strategy and geographic distribution (i.e., boreal or

austral). Red bars correspond to partially migratory species and black bars respresent

fully migratry species.

Table legends:

TABLE 1.

Models tested under the

Mk

model allowing and disallowing transitions

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TABLE2.

Partial migration is an intermediate step in the evolution between sedentary

and migratory species.

Support for the sequence of character state transitions under the

Threshold model calculated based on Deviance Information Criterion (DIC).

TABLE S1.

Sequences downloaded from PhylotaBrowser for each gene indicating the

lineage, the Gen Bank ID and the length of the sequence (bp).

(29)

Figure1.

(30)

!

M

igratory

P

artial Migrant

S

edentary

7.2

30

52.6

9.8 3.7e-07

3.7e-07

B.

(31)

(32)

Figure 3.

1

2

3

4

5

6

7

8

9

10

0.0

0.2

0.4

0.6

0.8

1.0 Model

Su

pp

ort

(w

AI

C

o

r

w

BI

C

)

wAIC

wBIC

M P S M P S M P S M P S M P S M P S M P S M P S M P S M P S

Mk model

M= Migrant; P= Partial Migrant; S= Sedentary

Su

p

o

rt

(w

A

IC

a

n

d

w

B

IC

)

(33)

Figure 4.

0.5

1.0

1.5

2.0

2.5

3.0

3.5

4.0

4.5

0.0

0.2

0.4

0.6

0.8

1.0 Model

Su

pp

ort

(w

AI

C

o

r

w

BI

C

)

λ

S

≠λ

P

≠λ

M

λ

S

=

λ

P

=

λ

M MuS=MuP=MuM MuS≠MuP≠MuM

λ

S

=

λ

P

=

λ

M MuS≠MuP≠MuM

λ

S

≠λ

P

≠λ

M MuS=MuP=MuM

Model

AICw BICw A.

(34)

Figure 5.

(35)

Tables:

Table1.

Model Mk model conditions

1 Allows all transitions

2 Forces transitions through partial migration

3 Constrains transitions from sedentary to migratory only

4 Constrains transitions from a migratory to a sedentary state only

5 Constrains transitions between migratory state and partially migratory states (in both directions) 6 Constrains transitions from sedentary to a partially migratory state only

7 Constrains transitions from partially migratory to a sedentary state only

8 Constrains transitions between sedentary and partially migratory states (in both directions) 9 Constrains transitions from partially migratory to a migratory state only

10 Constrains transitions from migratory to a partially migratory state only

Table2.

Model DIC value _2.5% _97.5%

M↔P↔S -410.8278 -495.101 -83.577 P↔M↔S -398.6321 -466.747 -22.578 M↔S↔P 208.9798 34.190 1167.246

Table S1.

NCBI taxon name GenBank ID

Sequence Length (bp) Beta-fibrinogen gene, intron 5

Agriornis murinus 383174977 491

Antilophia galeata 28630407 549

Atalotriccus pilaris 83031525 560

Camptostoma obsoletum 170877958 531

Capsiempis flaveola 83031577 557

Cnemotriccus fuscatus 167781948 582

(36)

Cnipodectes subbrunneus 83031531 561

Colonia colonus 83031529 558

Contopus cinereus 157780416 582

Corythopis torquatus 83031535 560

Corythopis torquatus 83031533 560

Elaenia albiceps albiceps 167782048 582

Elaenia albiceps chilensis 167782044 567

Elaenia albiceps griseogularis 167782062 584

Elaenia cherriei 167782029 584

Elaenia cherriei 167781966 554

Elaenia chiriquensis 83031537 562

Elaenia chiriquensis albivertex 167781892 585

Elaenia chiriquensis albivertex 167781890 550

Elaenia chiriquensis brachyptera 167781888 585

Elaenia cristata 167781990 540

Elaenia cristata 167782004 580

Elaenia dayi 167781986 546

Elaenia fallax fallax 167781984 553

Elaenia flavogaster 240018522 560

Elaenia frantzii 167781980 553

Elaenia frantzii 167782025 586

Elaenia gigas 167781994 528

Elaenia gigas 167781992 554

Elaenia martinica 167781988 553

Elaenia martinica 167781978 555