737

Biol. Rev. (2019), 94, pp. 737–752.
doi: 10.1111/brv.12476

A long winter for the Red Queen: rethinking
the evolution of seasonal migration
Benjamin M. Winger∗ , Giorgia G. Auteri, Teresa M. Pegan and Brian C. Weeks
Museum of Zoology and Department of Ecology and Evolutionary Biology, University of Michigan, Ann Arbor, MI 48109, U.S.A.

ABSTRACTThis paper advances an hypothesis that the primary adaptive driver of seasonal migration is maintenance of site fidelity
to familiar breeding locations. We argue that seasonal migration is therefore principally an adaptation for geographic
persistence when confronted with seasonality – analogous to hibernation, freeze tolerance, or other organismal
adaptations to cyclically fluctuating environments. These ideas stand in contrast to traditional views that bird migration
evolved as an adaptive dispersal strategy for exploiting new breeding areas and avoiding competitors. Our synthesis
is supported by a large body of research on avian breeding biology that demonstrates the reproductive benefits ofbreeding-site fidelity. Conceptualizing migration as an adaptation for persistence places new emphasis on understanding
the evolutionary trade-offs between migratory behaviour and other adaptations to fluctuating environments both within
and across species. Seasonality-induced departures from breeding areas, coupled with the reproductive benefits ofmaintaining breeding-site fidelity, also provide a mechanism for explaining the evolution of migration that is agnostic
to the geographic origin of migratory lineages (i.e. temperate or tropical). Thus, our framework reconciles much of theconflict in previous research on the historical biogeography of migratory species. Although migratory behaviour andgeographic range change fluidly and rapidly in many populations, we argue that the loss of plasticity for migration
via canalization is an overlooked aspect of the evolutionary dynamics of migration and helps explain the idiosyncratic
distributions and migratory routes of long-distance migrants. Our synthesis, which revolves around the insight that
migratory organisms travel long distances simply to stay in the same place, provides a necessary evolutionary context forunderstanding historical biogeographic patterns in migratory lineages as well as the ecological dynamics of migratory
connectivity between breeding and non-breeding locations.
Key words: geographic range, evolution of migration, site fidelity, philopatry, migratory connectivity, seasonality,
dispersal.
CONTENTS
I. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 738
II. Definitions of ‘migration’, ‘dispersal’, and the ‘evolution of migration’ . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 738
III. A brief history of theory on the evolution of bird migration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 739(1) Traditional paradigms for the evolution of migration tether biogeographic origin with mechanism . . 739(2) A geographically agnostic framework for the evolution of migration . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 740
IV. Adaptations to fluctuating environments, site fidelity, and the evolution of migration . . . . . . . . . . . . . . . . . . . . 741(1) Migration is an adaptation for persistence in seasonal environments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 741(2) Breeding site fidelity, not exploration, underlies the evolution of migration . . . . . . . . . . . . . . . . . . . . . . . . . . 743
V. Reconciling seasonal migration and geographic range evolution . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 745(1) Migration evolves similarly regardless of biogeographic origin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 745(2) Dispersal, tropical niche conservatism and the colonization of seasonal environments . . . . . . . . . . . . . . . 745(3) The evolution and persistence of disjunct geographic ranges in long-distance migrants . . . . . . . . . . . . . . 746
VI. Synopsis: a long winter for the Red Queen . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 748
VII. Conclusions . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 748
VIII. Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 749
IX. References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 749* Address for correspondence (Tel: ++1 734 763 3379; Fax: ++1 734 763 0544; E-mail: wingerb@umich.edu).
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I. INTRODUCTION
When an animal finds a suitable location for reproduction,
there are benefits to continuing to breed in that location year
after year. The challenges of resource acquisition, predator
evasion and interactions with competitors are lessened byintimate familiarity with a breeding territory, whereas leaving
a territory puts an individual at risk of losing the location
to a competitor and also subjects it to an unfamiliar terrain
containing different parasites, pathogens and predators (Pärt,
1995; Bensch et al., 1998; Doligez & Pärt, 2008; Altizer, Bartel& Han, 2011; Bonte et al., 2012). Yet, every year, billions ofadult animals leave the localities where they invested heavily
in the acquisition and defence of a breeding territory tojourney across the globe. Some will next breed in new sites
wherever and whenever resources allow, but among birds,
these nomadic species are a minority (Winkler, 2005). Rather,most of the birds that vacate their breeding territories in one
season will, in a matter of months, attempt to return to thesame locales where they bred before. These are the migratory
species, whose seasonal drive towards specific breeding sites
is all the more remarkable given the long distances they
travel between breeding events.
Seasonal migration can be understood intuitively as apersistence strategy, allowing an organism to achieve thebenefits of maintaining a breeding territory while avoiding
the fitness or survival cost of a resource-depleted season
in that location (Bell, 2000; Alerstam, Hedenstrom &Akesson, 2003; Cresswell, Satterthwaite & Sword, 2011).
Migration is just one of many possible adaptive strategies thatenable persistence and continued reproduction in seasonalenvironments. Other organisms employ analogous strategies
for coping with pronounced seasonality as diverse as
hibernation, diapause, changes in diet and social behaviour,or physiological changes to improve freeze tolerance. As with
migration, the complexity and degree of other adaptations
to fluctuating environments is predicted by the severity ofseasonality in different regions (Williams et al., 2017), but allorganisms found in seasonal environments must have some
adaptation for predictable intra-annual changes in climate
and food resources or they will not persist. Seasonal migrationand other adaptations for seasonality, such as hibernation,
thus have a similar adaptive function: to maintain access tobreeding territories that experience predictable periods ofresource depletion.
Contrary to this perspective, seasonal migration in birds
has often been viewed not as having evolved to facilitate
persistence in a seasonal environment, but rather as acolonization strategy for finding new breeding sites with fewer
competitors, less formidable predators and more abundantfood resources than supposedly more crowded and dangerous
tropical locales (Cox, 1968, 1985; Levey & Stiles, 1992;
Safriel, 1995; Rappole & Jones, 2002). This framework
has resulted in a problematic linkage of the geographic
origins of lineages that contain migratory species and themechanisms proposed to explain the evolution of migratory
behaviour in birds (Salewski & Bruderer, 2007; Winger,
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Benjamin M. Winger and others
Barker & Ree, 2014). Moreover, in the ornithologicalliterature, this perspective has typically precluded migrationin birds from being considered within a broader context ofother organismal – and even other avian – adaptations toseasonality and fluctuating environments.
In this synthesis, we advocate a change of perspective
to view the evolution of seasonal migration in birds
principally as an adaptation for persistence in a seasonalenvironment – analogous to alternative adaptations such ashibernation. This view provides an improved framework forunderstanding both the mechanisms by which bird migration
evolves as well as its inherently complex relationship withthe evolution of geographic ranges. Although migration
is widespread and highly variable across many groupsof animals (Dingle, 2006; Shaw, 2016), we focus on the
migrations of birds and in particular their regular, cyclical,
seasonal migrations. An improved understanding of bird
migration and its influence on avian biogeographical patterns
will inform the study of migration in other animal groups,
including the accentuation of differences in migratory
strategies across taxa.

II. DEFINITIONS OF ‘MIGRATION’, ‘DISPERSAL’,
AND THE ‘EVOLUTION OF MIGRATION’
We consider migration a regular, seasonal round-trip
movement between a region where young are reared (a‘breeding range’) and a non-breeding region or regions. By
contrast, dispersal, a phenomenon found in all species to somedegree, is a one-way movement of an individual between
breeding locations. In birds, even those with long-distancemigrations, dispersal typically occurs over short distances, asbirds have high fidelity to their breeding sites. Usually, it is
only the first dispersal event of a bird’s lifetime – from thelocation in which a bird was hatched to where it first breeds(natal dispersal) – that occurs over any appreciable distance.
In subsequent breeding seasons, an individual bird is likely toreturn to the same breeding site that it used in the previous
year. Philopatry refers specifically to the tendency to return tonatal sites, whereas breeding-site fidelity refers to the tendency toreturn to the site where an adult individual bred previously.
Individuals may also maintain fidelity to wintering andstopover locations or change these locations throughout their
lifetimes; thus, changes to non-breeding sites throughout thelife of an individual could be considered dispersal, but for thesake of consistency with previous literature we use the term
‘dispersal’ to refer only to changes in breeding location.
Migratory movements are highly variable across birds.
Species in which only some individuals within a population
migrate or wherein populations are variable in migratory
behaviour are known as partial migrants, in contrast to complete or obligate migrants. The cyclical regularity of seasonal
migration stands in contrast to facultative migrations such asnomadism and irruption, both of which are irregular phenomena. Nomadic behaviour occurs in species that vary theirbreeding sites and often their timing of breeding according

The evolution of seasonal migration
to the unpredictable availability of resources, resulting in
irregular movements of portions of the population. Irruptive
movements occur when birds move away from their breeding sites during times of low resource availability, but unlike
seasonal migration, irruption occurs irregularly depending
on food resources and population dynamics. In some species,
irruption and nomadism are difficult to distinguish, and inother species the lines may be blurred between migrationand nomadism or irruption (Eyres, Böhning-Gaese & Fritz,2017). Nomadism is often considered to be a variation of
migration (e.g. Newton, 2010), but the differences in the roleof breeding-site fidelity between these two behaviours – innomadism, a repeated movement to a new breeding
territory, and in migration, a repeated return to a single
breeding location – suggests that nomadism is perhaps bestthought of as sequential dispersal (Boyle, 2018).
We refer frequently to the ‘evolution of migration’. Zink
(2002, 2011) has cautioned that the ‘evolution of migration’in a lineage should not be confused with the ‘origin’ of
migratory behaviour. Zink suggests that because migration is
likely an ancient aspect of avian biology that has been gained
and lost repeatedly in the avian tree of life through selection
on existing genetic composition as opposed to de novo
evolution in different lineages, that the phrase ‘evolutionof migration’ is problematic. We agree with Zink’s pointthat the appearance of migratory behaviour in a populationthat was previously sedentary does not mean that migration
originated de novo. When using the phrase ‘evolution of
migration’, we simply mean the appearance or intensification of
migratory behaviour in a population or lineage that was previously
sedentary or less migratory, regardless of underlying molecular
evolution or putative homology.

III. A BRIEF HISTORY OF THEORY ON THE
EVOLUTION OF BIRD MIGRATION(1) Traditional paradigms for the evolution of
migration tether biogeographic origin withmechanism
The inherently complex geography of seasonal migration
has led to much debate about how to reconcile mechanistic
aspects of the evolution of bird migration with thebiogeographic history of migratory lineages (Zink, 2002;
Salewski & Bruderer, 2007; Winger et al., 2014). Theories on
the evolution of bird migration have already been extensively
reviewed (e.g. Gauthreaux, 1982; Rappole & Jones, 2002;
Salewski & Bruderer, 2007; Boyle, 2018), and several themes
have emerged that have had a persistent influence on our
understanding of the relationship between the evolutionof migration and geographic range dynamics. Because themost dramatic bird migrations occur across latitudes, theevolution of bird migration has often been framed as a‘southern-home’ versus ‘northern-home’ debate, which canbe generalized to a ‘tropical home’ versus ‘temperate home’framework to include austral migration. According to the739
tropical home paradigm, contemporary migrations between
temperate and tropical latitudes evolved in tropical birds
as a mechanism to take advantage of bountiful resources
and fewer competitors in temperate regions (Rappole, 1995;
Safriel, 1995; Rappole & Jones, 2002). These ideas stem
largely from Cox (1968), who argued that seasonal migration
evolves in tropical, sedentary birds that are driven bycompetition to move into adjacent, higher latitude habitats
to breed. Cox (1968, p. 183) wrote, ‘given permissive
conditions, selection should favour any . . . variation leading
to incipient migratory movements into adjacent areas
if the reduction in total competition (intraspecific andinterspecific) allows greater survival or reproduction . . . thanin the original [sedentary] range’. In other words, thetemperate zone was considered more favourable for breeding
than the tropics and organisms should evolve to migrate
there. Importantly, Cox suggested that the first migrations(‘incipient migratory movements’) involved movements outof tropical or subtropical areas to colonize new breeding
locations in more seasonal, temperate areas. Although it
was implicit that the harsh, resource-depleted winters in thebreeding ranges of temperate migratory birds forced themto return every year to the tropics, Cox considered a lackof resources in the winter to be of lesser importance to theevolution of migration than the bounty of resources and lackof competitors in temperate-latitude summers.
The related but distinct ‘evolutionary precursor’
hypothesis also envisioned migration evolving out of thetropics via an initial migration to a higher latitude breeding
location where reproductive success would be greater,and suggested that certain diets or habitats predisposedsome tropical lineages to become migratory (Levey &Stiles, 1992; Chesser & Levey, 1998; Boyle & Conway,2007). Specifically, frugivory and nectarivory were seenas ‘evolutionary precursors’ to seasonal migration, as waspreference for edge habitats, because the search for these
spatially ephemeral foods and habitats might lead to longer
distance movements (Levey & Stiles, 1992). As with theother tropical home hypotheses, the evolutionary precursor
hypothesis envisioned the incipient migratory movements ina sedentary tropical ancestor as occurring from ancestral
tropical breeding areas to more seasonal, higher latitude
breeding areas. A return trip to the tropics was implicitly
driven by a lack of resources in high-latitude winters but was
not viewed as having stimulated the evolution of migration.
Support for tropical home theories increased in parallelwith the growth of ecological knowledge about tropicalmigrants on their wintering grounds. As tropical ecologists
learned that Neotropical migratory birds that breed athigh latitudes have intricate ecological relationships withresident tropical species during northern winters (e.g. Keast& Morton, 1980; Holmes, Sherry & Reitsma, 1989), theconviction strengthened that these migrants must haveoriginated in the tropics (Levey & Stiles, 1992; Rappole &Tipton, 1992; Levey, 1994). Recognition that short-distancemovements (such as altitudinal migration) are much morecommon among tropical birds than previously supposed also
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bolstered support for tropical origins of migration (Levey,
1994; Jahn, Levey & Smith, 2004; Boyle & Conway, 2007).
In recent literature, tropical home theories have frequently
been presented as the consensus view (e.g. Jahn et al., 2004;
Pulido, 2007; Bisson, Safi & Holland, 2009), resulting in
the widespread framing of long-distance migration as a
strategy to escape competition in the crowded tropics or
to increase reproductive success through exploitation ofenergy resources during high-latitude summers (Rappole& Jones, 2002; Guttal & Couzin, 2010; Somveille, Rodrigues& Manica, 2015, 2018b; Turbek, Scordato & Safran, 2017).
Although seasonality has clearly been recognized as
an important aspect of migration (Alerstam et al., 2003),
theories of the evolution of migration involving selection
to avoid the harsher, resource-limited aspects of seasonalenvironments (as opposed to exploit beneficial aspects) havereceived surprisingly limited consideration, considering theintuitiveness of this idea. Alfred Russel Wallace (Wallace,1874) and Ernst Mayr [Mayr & Meise, 1930, in Salewski& Bruderer, 2007] suggested that a lack of resources intemperate winters drove the evolution of migration, but few
recent authors other than Bell (2000, 2005) and Salewski &Bruderer (2007) have championed these beliefs. Retreat fromdeteriorating seasonal conditions in temperate winters has
been viewed more as an incidental consequence of migration,rather than a cause.
Resistance to viewing seasonality as the principal driver ofthe evolution of migration, despite the obvious connection,
was in part due to the tethering of the biogeographic origin of
migration (i.e. tropical versus temperate home) with the selective pressures that stimulate migration (Zink, 2002; Salewski& Bruderer, 2007). That is, if a migratory lineage was thought
to be of tropical origin, it was assumed that the selection pressures leading to migration must have occurred in the tropics(e.g. Rappole, 1995; Rappole & Jones, 2002). However, ourunderstanding of the biogeographic origins of migratory
lineages has been obscured by the complex biogeography
inherent to seasonal migration (Joseph, Lessa & Christidis,
1999; Winger et al., 2014). Consequently, progress towards
clarifying the selective pressures underlying the evolution of
migration has been hindered by confusion surrounding therelationship between the geographic origins of migratory
lineages and the mechanism by which migration evolves.
(2) A geographically agnostic framework for theevolution of migration
Salewski & Bruderer (2007) advanced theory on theevolution of migration considerably by articulating the major
shortcomings of the ‘southern’ or ‘tropical home’ theories
and calling into question the necessity for a connection
between the biogeographic origin of migratory lineages
and the evolution of migration. The central problem they
identified was a conflation of dispersal and migrationin previous theories. Dispersal is a movement whereby
individuals search for and find new breeding sites (seeSection II), and the geographic range expansion of ataxon is an emergent property of successful dispersal of
Biological Reviews 94 (2019) 737–752 © 2018 Cambridge Philosophical Society

Benjamin M. Winger and others
individuals. High population density may select for more
highly dispersive behaviour, suggesting a connection between
competition and dispersal patterns (Matthysen, 2005; Coteet al., 2017). However, density-dependent dispersal is distinct
from seasonal migration; that is, there is not a clear
conceptual basis for why high competition in a region
would lead directly to regular movement not only away
from, but also back to, the ancestral region, as suggested
by tropical home theories (Bell, 2005; Salewski & Bruderer,2007). Furthermore, the rationale underlying the expectationthat there are adaptive benefits for migration away from thetropics to new breeding sites in temperate regions restedon the supposition that the reproductive success of birds isgreater at higher latitudes. Such life-history theory, which
was based largely on clutch-size variation across latitudes,
is now known to be an oversimplification; relying only
on clutch size or fecundity to define reproductive successoverlooks nuances of avian developmental biology andmortality across latitudes that create trade-offs between
lifetime versus single-season reproductive success (Martin,
2004, 2015; Salewski & Bruderer, 2007).
To disentangle the evolution of migration from thebiogeographic history of migratory lineages, Salewski &Bruderer (2007) proposed the geographically agnostic‘dispersal-migration-theory’ in which regular dispersal fromless-seasonal areas into more-seasonal areas, regardlessof geographic orientation, precedes and facilitates theevolution of migratory behaviour. That is, when individuals
from a sedentary population disperse away from theirnatal territories and establish in new locations, they maycolonize adjacent areas that are more seasonal than theancestral region. Natural selection would then favour theevolution (or expression; see Section II) of migration in
the newly colonized region as an escape strategy to avoid theharsher, resource-depleted season (Fig. 1). Thus, migrationand geographic range evolve in tandem. That selection
for migration in a seasonal environment should increase
the proportion of migrants in a population was not a new
idea – this is the basis of the ‘threshold model’ for the evolution of migration (Berthold, 1999). However, the influence ofdispersal, rather than migration, in facilitating the expansionof populations into more seasonal environments had notbeen fully articulated. Consequently, prior to Salewski& Bruderer (2007), the threshold model had not beenadequately contextualized with respect to the biogeographic
changes that can accompany the evolution of migration.
Salewski & Bruderer’s (2007) ‘dispersal-migration-theory’
thus provided a useful entry point for conceptualizing
the evolution of migration and its relationship to theevolution of geographic range. Here, we build on theideas that migration originates either through dispersal
into seasonal environments or through in situ changes
in seasonality through time (Fig. 1; Bruderer & Salewski,
2008; Louchart, 2008) by adding two critical componentsthat typically have not been connected to the evolutionof migration: (i) we highlight the importance of viewing
migration not only as an adaptation for persistence inThe evolution of seasonal migration

741

(A)
High

Seasonality across space

B

x

Low
1: breeding or natal dispersal

2: response to encountered seasonality

3: seasonally adapted populations

(B)
x

x
x

x
x

1: aseasonal environment

2: range becomes more seasonal

3: seasonally adapted populations

Fig. 1. The evolution of migration in response to seasonality. (A) Migration may evolve following dispersal into a seasonalenvironment. Our depiction builds on Fig. 2 from Salewski & Bruderer (2007). Panel 1: individuals that are found in relatively
aseasonal environments, or the offspring of these individuals, may disperse (arrows) into environments that are more seasonal in
the course of regular, undirected searches for new breeding locations. Panel 2: when seasonal conditions deteriorate in the newly
occupied region (i.e. during winter), individuals (orange) that escape via movement (dashed arrow) to a more hospitable non-breeding
territory (blue) may have a better chance of survival. Panel 3: owing to the selective benefits of breeding-site fidelity, selection
will favour individuals that return to their previous breeding region, and thus migration (dashed arrows) will typically be favoured
over nomadism in predictably fluctuating (i.e. seasonal) environments. Alternatively, individuals that adopt a different adaptation
to seasonality that does not involve movement, such as hibernation (pink), may also survive and breed again near their previous
breeding location. However, individuals that do not display any physiological or behavioural modification for increased seasonality
will not survive or will have lower fitness (red). Over time, either round-trip migrations (orange and blue) or adaptations such ashibernation (pink) may enable species to colonize yet more seasonal regions and the relative prevalence in a population of migration
versus other adaptations to seasonality will depend on numerous factors including phylogenetic history, physiological constraints,
and behavioural plasticity. (B) Similarly, migration may evolve in response to increased seasonality through time. As aseasonalenvironments become more seasonal across years, only individuals that migrate or evolve alternative adaptations to seasonality will
persist.

a seasonal environment but as one of many alternative
organismal adaptations to seasonality; and (ii) we posit thatbreeding-site fidelity – a phenomenon observed widely inmany animal taxa – underlies the origin and maintenanceof migratory behaviour as an adaptive strategy. This latter
point stands in contrast to the perspective that aligns theevolution of migration with exploratory dispersal to new
breeding sites, rather than site fidelity. We then discuss how
this new perspective on the adaptive function of migration
represents an important but largely overlooked consideration
for understanding biogeographic patterns in migratory taxa
such as birds, including the idiosyncratic and extreme range
disjunctions of long-distance migratory species that have long
perplexed biogeographers.

IV. ADAPTATIONS TO FLUCTUATINGENVIRONMENTS, SITE FIDELITY, AND THE
EVOLUTION OF MIGRATION(1) Migration is an adaptation for persistence inseasonal environments
Reviews of bird migration often begin by giving credit
to Aristotle for the earliest known scientific treatment of
the topic, to highlight humanity’s long fascination withthe migrations of birds (Thomson, 1926; Wetmore, 1930;
Gauthreaux, 1980; Milner-Gulland, Fryxell & Sinclair, 2011;
Boyle, 2018). Some authors go on to give Aristotle amore ignominious attribution by mentioning that he was
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742
the first writer to hypothesize that birds had a different
strategy for surviving the winter: hibernation. Throughout
the Middle Ages and into the nineteenth century, thebelief persisted that swallows hibernated in the mud ofrivers and marshes (Thomson, 1926). As twentieth century
ornithologists learned more about bird migration, theories
of hibernation were dismissed with derision, and Aristotle’s
association with advancing such theories was regarded as
something of an embarrassing lapse in omniscience. For
example, Wetmore (1930) discussed avian hibernation in asection titled ‘Theories of Migration: Superstitious Beliefs’,in stark contrast to the next section of his book, ‘ScientificHypotheses of Migration’. Thomson (1926, p. 23) wrote withrespect to avian hibernation that with ‘better knowledge ofbird-migration [sic] it is now possible to dismiss these theories
as lightly as those once popular notions that birds became
transformed into other species in winter or that there is
migration between the Earth and the Moon’.
Today, the scientific literature on the evolution of
bird migration almost never mentions hibernation as
an alternative to migration – not even as a target of
ridicule – because we now know with certainty that birds
migrate long distances and we understand that subterraneanhibernation is a decidedly non-avian behaviour. Yet, it
turns out that one species of bird (the Common Poorwill,
Phalaenoptilus nuttallii) sometimes hibernates in the high, cold
deserts of western North America (Jaeger, 1948, 1949;
Brigham, 1992). Other avian species (albeit from only ahandful of lineages) undergo daily torpor (Geiser, 2004).
Many more species have shallower facultative hypothermic
responses for energy conservation (McKechnie & Lovegrove,
2002; Ruf & Geiser, 2015; Douglas, Cooper & Withers,2017) or adjust metabolic rate to survive cold temperatures(Swanson & Garland, 2009; Swanson & Vézina, 2015; Stager
et al., 2016). Beyond migration and adjustments to metabolic
rate, avian adaptations to withstand cold temperatures arediverse. For example, 6-g kinglets survive boreal winternights at temperatures of −40◦ C by huddling together;grouse and ptarmigan make snow burrows; cavity-nesting
birds may roost within their nest holes, sometimes socially;
many finches have evolved flexible breeding schedules andentirely granivorous diets that allow them to exploit foodresources year-round at high latitudes; and certain lineages
such as corvids are capable of profound seasonal shifts intheir social behaviour, foraging, and diet (Stutchbury &Robertson, 1990; Heinrich, 2003a,b; Gill, 2007).
By banishing avian hibernation to the realm ofscience fiction, early thinkers on the evolution of
migration divorced bird migration from this rich diversityof other physiological and behavioural adaptations toseasonal environments – adaptations that are important forunderstanding bird migration because they represent thenecessary alternatives to migratory behaviour if a lineage
is to persist in a highly seasonal region (Lyman et al.,
1982; Sol, Lefebvre & Rodriguez-Teijeiro, 2005). Thisdecoupling of migration from other adaptations to seasonality
was perpetuated throughout the 20th century literature on
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Benjamin M. Winger and others
bird migration. Because bird migration between temperate
and tropical latitudes was conceptualized as a movement
stimulated initially by in situ tropical selection pressures(e.g. Cox, 1985; Levey & Stiles, 1992), as opposed to a
behaviour conferring a selective advantage in a population
found in a seasonal environment, migration was not regarded
as an adaptation for persistence akin to other organismal
adaptations to seasonality.
We propose that a more useful framework recognizes
that migration is an adaptation for increasing fitness inthe face of fluctuations in climate or resources. Because ofthis, the proportion of migratory species in a region scales(broadly) with the severity of resource fluctuations (Somveilleet al., 2013, 2018b). That is, short-distance migrations occur
in the tropics and are driven by seasonal dynamics such as
wet-dry cycles, but the greater severity of seasonality at higher
latitudes drives the evolution of migrations that are not only
more extreme in geographic scope but also comprise a larger
proportion of the regional avifauna (Gómez et al., 2016).
Furthermore, the concept that unites migration with otherorganismal adaptations to seasonality is the recognition thatthe absence of migration in a highly seasonal environment
is not, in itself, a viable alternative to migration. Rather,
the absence of migration in a species that lives in a highly
seasonal environment necessarily signifies the existence ofan alternative adaptation to seasonality in that species.
Likewise, in partially migratory species, individuals that do
not migrate or that migrate facultatively must also haveadaptations to overcome the consequences of not migrating(Chapman et al., 2011; Fudickar et al., 2016). Depending on
the ecological context, the absence of migration may requirea profound behavioural or physiological shift during theannual cycle (such as social roosting in territorial species
or dietary shifts to granivory in insectivores) or relatively
subtle changes (such as an adjustment in the species of fruit
consumed at different times of year in the tropics; Boyle,
Conway & Bronstein, 2010). Recognition that obligate,
long-distance migration is one of several possible migratory
responses to seasonality (including altitudinal or facultative
migrations), but moreover that all migratory movements
collectively represent an alternative to yet other adaptations
to seasonality that do not involve geographic escape, is anecessary context for understanding how and why different
adaptations to fluctuating environments evolve.
Given the diversity of possible responses to seasonality,
why is migration the most common strategy in birds,
and why does migration evolve more frequently in somelineages than others? Certainly, the vagility of birds andother volant organisms predisposes them for migration.
Yet, birds have great variation in the degree to which
they use their wings for locomotion (Heers & Dial, 2015),
suggesting the commonness of migration among birds ismore reflective of the evolutionary lability of the avian flightapparatus (including associated metabolic, physiological andneurological accommodations for long-distance flight) thanthe existence of a flight apparatus per se. Such evolutionary
flexibility of the flight apparatus stands in apparent contrast

The evolution of seasonal migration
with the lability of another structure possessed by all
birds: the brain. Sol et al. (2005, 2010) provided evidence
for larger brains in resident versus migratory species, andargued that year-round persistence in a highly seasonalenvironment requires a larger brain that allows for greater
flexibility in diet and behaviour necessary to survive in aresource-depleted landscape. This idea has been debated, inpart due to the difficulty of determining whether the smaller
brains of migrants are truly representative of neurologicaldeficiencies or are a consequence of the energetic demandsof migration selecting for smaller crania (Winkler, Leisler &Bernroider, 2004; Pravosudov, Sanford & Hahn, 2007; Sayol
et al., 2016; Fristoe, Iwaniuk & Botero, 2017). Additionally,
migratory species may also change their diets throughout
the year (e.g. Gómez et al., 2018). Nevertheless, many
bird species that maintain year-round occupancy in theenvironments with the greatest fluctuation in resource baseare those that have evolved neurological adaptations for foodcaching (Sherry et al., 1989) or extreme flexibility in diet,often facilitated by complex social interactions (Marzluff,
Heinrich & Marzluff, 1996). As migration is a much morecommon adaptation to seasonality in birds, transitions to ahighly migratory lifestyle seem more likely to evolve quickly
and repeatedly than evolutionary changes in neurobiologythat would facilitate alternative behavioural flexibilities for
persistence in environments with extreme competition for
depleted resources. Parallel arguments can likely be madefor the relative rarity of other behavioural and physiological
adaptations to seasonality, such as hibernation. Although
the reasons why adaptive hypothermia is rare in birds
are not well understood (McKechnie & Lovegrove, 2002;
Ruf & Geiser, 2015), the high evolvability of avian vagility
combined with a relatively low flexibility of metabolic rates
in birds has likely led to migration evolving more commonly
in birds than, for example, small mammals or amphibians.
Other highly vagile organisms such as bats and insects
have also evolved migration repeatedly, but combine theirmigrations with other strategies such as torpor and dormancy
in complex ways whose evolutionary history demands further
investigation (Bisson et al., 2009; Shaw, 2016)
There is a great deal we have yet to learn about why
certain adaptations for seasonality evolve only in somelineages, or manifest only in some individuals, and what
evolutionary trade-offs are involved in different strategies.
To date, discussions of these trade-offs have mostly takenplace in the literature on partial migration, in the context ofunderstanding intraspecific variation in migratory behaviour
among individuals (e.g., Ketterson & Nolan, 1982; Boyle,
2011; Chapman et al., 2011; Zúñiga et al., 2017). Interspecificcomparisons, framed in the context of alternative butfunctionally similar adaptations for persistence in a seasonalenvironment, are also important for understanding theevolution of migration and other adaptive strategies forseasonality. For example, the 16-g Blackpoll Warbler(Setophaga striata) flies 4 days nonstop from breeding grounds
in the boreal forest to winter locations in the Amazon (Fig. 2;
Deluca et al., 2015). By contrast, the 6-g Golden-crowned

743
Kinglet (Regulus satrapa) often spends the northern winter nearthese same boreal breeding grounds (Fig. 2; Heinrich, 2003a).
Both of these strategies, migration and residency, involve
profound seasonal shifts in diet, physiology, behaviour andpathogenic regimes. The long-distance migration of theBlackpoll Warbler is rightly celebrated as an extraordinaryfeat of endurance, but this strategy has actually evolved
more frequently across the avian tree of life than thepersistence strategy used by the kinglet. Recognition thatseasonal migration is one of several possible adaptations for
persistence in any seasonal environment promises to advanceour understanding of the evolutionary trade-offs between
migratory behaviour and other adaptations to resource
fluctuations in birds and other organisms.
(2) Breeding site fidelity, not exploration, underlies
the evolution of migration
It is intuitive that an animal might leave an area when climaticconditions become unfavourable and resources scarce: forsome populations (or for some individuals in populations
with mixed migratory strategies), leaving a region in the
non-breeding season offers a greater probability of survival
than staying, despite the costs of migration (Lack, 1968;
Zúñiga et al., 2017; Dokter et al., 2018). Indeed, migration istypically described as a resource-tracking strategy (Alerstam
et al., 2003; Alerstam & Bäckman, 2018; Somveille et al.,2018b). But why should migrants return the following spring,rather than settle on their non-breeding grounds or disperse
to a new breeding location with yet better resources, as do
nomadic species? This question has usually been answeredby defining migration as an endogenously driven round trip,
but a satisfying exploration of the selective forces that led
to this endogenous control has been elusive (Berthold, 1999;
Salewski & Bruderer, 2007).
We propose that a central conclusion from a long
history of research on the breeding biology of migratory
birds provides the needed explanation for the mechanism
underlying selection for a regular, round-trip migration: itis the increased reproductive success leveraged by efficiently
returning to successful breeding sites, as opposed to thedrive to disperse to potentially better breeding sites outside
a species’ range (as predicted by tropical home theories),that underlies the endogenous control of seasonal migration
as a round trip. Many studies have shown that individual
birds that arrive quickly at their breeding grounds havehigher reproductive success than birds that arrive and begin
nesting late (Perrins, 1970; Price, Kirkpatrick & Arnold,
1988; Marra, Hobson & Holmes, 1998; Kokko, 1999; Norris
et al., 2004; Charmantier & Gienapp, 2014). Arriving on timeto the breeding grounds should be easier when the location is
known, resulting in selection for fidelity to successful breedingsites in returning breeders (Greenwood & Harvey, 1982;
Payne & Payne, 1993; Pärt, 1995; Hoover, 2003; Hansson,
Bensch & Hasselquist, 2004). Individuals that do not migrate
thus gain the reproductive advantage of staying near to theirbreeding sites or having more time to search for nearby sites(Chapman et al., 2011; Kokko, 2011; Zúñiga et al., 2017). But
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744

Regulus satrapa

Setophaga striata

Zonotrichia albicollis

Fig. 2. Variations in migratory strategy reveal alternative adaptations to seasonality. The diminutive Golden-crowned Kinglet(Regulus satrapa) breeds in boreal North America (red), with resident populations (purple) and wintering populations (blue) persistingyear-round in harsh boreal environments. By contrast, Blackpoll Warblers (Setophaga striata) undergo an arduous migration frombreeding grounds in boreal North America to wintering grounds in northern South America. White-throated Sparrows (Zonotrichia
albicollis) migrate short distances to take advantage of the less-harsh winters in the southern USA. Images reproduced with permission
from del Hoyo et al. (2018).

individuals that migrate are also under strong selection to
return rapidly to known breeding regions and re-establish
territories (Kokko, 1999), leading to migrations that tend tobe faster in in spring than in autumn (Horton et al., 2016).
Research on the wintering ecology of migratory birds
suggests that individual fidelity to wintering sites is also an
important component of migration in some species, withwinter site fidelity increasing over-winter survival and body
condition (Holmes et al., 1989; Holmes & Sherry, 1992;
Cresswell, 2014; Shizuka et al., 2014; Blackburn & Cresswell,2016). Importantly, behavioural and ecological traits thatbolster over-winter survival and condition of individuals must
translate to increases in reproductive success to be selected
for across generations. Therefore, although the ecologicaldynamics of the non-breeding season dictate many important
population-specific details of migratory behaviour, we argue
that natural selection fundamentally acts on the non-breeding
portions of the annual cycle to support an efficacious return
to familiar breeding grounds in spring. Indeed, increased
winter survival and fitness has been shown in some studies tobolster reproductive success the following spring (e.g. Sillett,Holmes & Sherry, 2000; Norris et al., 2004), highlighting
the importance of full-annual-cycle ecological research forunderstanding the population dynamics, migratory routes,
and biogeography of migratory birds (Marra et al., 2015).
Rapid changes to some migratory species’ ranges thathave been observed over recent decades could lead to theconclusion that migratory species are less site faithful than
we have claimed here. However, in species in which such
geographic shifts have been studied in detail, such as the
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Icelandic Black-tailed Godwit (Limosa limosa islandica), range
expansions typically occur via the dispersal of young birds
to their first breeding sites (i.e. natal dispersal) or wintersites, while adults maintain site fidelity to both breeding andwinter locations (Gunnarsson et al., 2005, 2006; Gill et al.,2013). In general, fidelity to natal sites among animals – bothmigratory and sedentary – carries costs as well as benefits
and most juvenile individuals must disperse away from theirnatal sites for their first breeding attempt (Winkler, 2005;
Studds, Kyser & Marra, 2008). Yet, most individuals disperse
short distances (Hosner & Winkler, 2007; Nathan et al., 2012),
and the adaptive value of preference for natal habitats, if not
specific natal sites, bolsters philopatric tendencies (Davis &Stamps, 2004; Stamps, Krishnan & Reid, 2005) and likely
contributes to selection for round-trip migrations. Thus, theexistence of natal dispersal in migratory birds should not
be interpreted as evidence against the profound influence of
selection for breeding-site fidelity later in life on structuring
the evolution of migratory and biogeographic patterns, evenwhen such dispersal facilitates range expansions or shifts.
Of course, not all migratory birds always exhibit
breeding-site fidelity from 1 year to the next. Variation
exists in breeding-site fidelity within and across species that
we are only beginning to understand due to the difficultyof detecting and measuring dispersal within species’ normal
ranges (Rushing et al., 2015; Kempenaers & Valcu, 2017;
Boyle, 2018; Williams & Boyle, 2018). At larger spatial scales,
long-distance ‘jump’ dispersal of adults has sometimes led todramatic (i.e. intercontinental) range expansion events (deQueiroz, 2014). And, occasionally, a migratory population

The evolution of seasonal migrationof birds does not come back to the original breeding grounds
but rather begins breeding on its wintering grounds. Thishas been observed directly over the course of just a few
generations (Winkler et al., 2017), and there is phylogenetic
evidence that such migratory ‘drop-offs’ may have occurred
regularly across macroevolutionary time scales (Kondo et al.,2008; Winger, Lovette & Winkler, 2012; Rolland et al., 2014).
But these exceptions prove the rule, by highlighting thatfor the vast majority of the time, natural selection favours
individuals that not only migrate away from their breeding
grounds when seasonal conditions deteriorate, but also return
again the next season to the same breeding regions and often
the same specific site where they raised young the year before.

V. RECONCILING SEASONAL MIGRATION AND
GEOGRAPHIC RANGE EVOLUTION
We have argued that dispersal, not migration, is themechanism that leads to range expansion into seasonal areas(Salewski & Bruderer, 2007). We have also proposed thatbreeding-site fidelity, not dispersal to new breeding sites,
is ultimately the driver of migration, and consequently thatseasonal migration principally serves the adaptive functionof maintaining familiar breeding territories in seasonalenvironments. Below, we explore how this perspective contributes to an understanding of the evolution of geographic
range as well as biogeographic and macroecological patterns
in lineages containing migratory species.
(1) Migration evolves similarly regardless ofbiogeographic origin
By distinguishing dispersal from migration, it becomes clearthat the biogeographic origin of a lineage need not be thesame as the geographic region where migration evolved(Salewski & Bruderer, 2007; Bruderer & Salewski, 2008).
For example, a sedentary tropical species may expand its
range into more temperate areas through gradual dispersal,
and in so doing, selection may cause the population to
become migratory in the portions of its range that are
more seasonal (Fig. 1). In this way, latitudinal migration
may evolve in a tropical lineage as it expands its range
poleward. That is, migration and geographic range evolve
reciprocally, such that a lineage will not persist in regionswith high seasonality unless it evolves migration (or analternative adaptation for seasonality; Fig. 1), and only
lineages exposed to pronounced seasonality will evolve
latitudinal migrations (Gómez et al., 2016). Shorter-distanceor facultative migrations, such as altitudinal migration(Boyle, 2011, 2017; Hsiung et al., 2018), may similarly evolve
anywhere there are seasonal selection pressures that confer
a fitness advantage to migration, including tropical areas
with seasonality in climate and resources. In addition to asedentary or partially migratory population becoming moremigratory by expanding geographically into a more seasonal
region, migration may also evolve as environments become

745
more seasonal through time (Fig. 1). Just as populations
undergoing range expansion into more seasonal areas will
only persist if they adapt to increased seasonality, populations
will only persist in situ if they adapt to temporal increases
in seasonality (Fig. 1; Bruderer & Salewski, 2008; Louchart,
2008; Winger et al., 2014).
Because the selection pressures that drive the evolution of
migration as populations expand their ranges across space
are the same as those that drive the evolution of migration as
seasonality changes through time, migration evolves throughthe same mechanisms regardless of the biogeographic originof the lineage (Bruderer & Salewski, 2008). For example,
Louchart (2008) suggested that the contraction of tropical
habitats to low latitudes during the Oligocene and Miocene
caused the evolution of migratory behaviour in some lineages
through the movement of winter ranges towards the equatorand persistence of breeding ranges at high latitudes. Thispremise was supported by a phylogenetic reconstruction ofbreeding and winter ranges in a large clade of New World
migratory birds, the Emberizoidea, which likely evolved
migration through shifts of winter ranges to tropical latitudes
from ancestral ranges in North America (Winger et al., 2014).
Also found in North America are highly migratory birds oftropical origin, such as Tyrant Flycatchers (Tyrannidae),which trace their biogeographic origins to South America
but have similar migratory patterns as many Emberizoids.
However, that the ancestors of some migrants were foundin the tropics does not necessitate invoking tropical hometheories for the evolution of migration (e.g. Outlaw et al.,
2003; Licona-Vera & Ornelas, 2017; O’Connor et al., 2018).
Rather, the ancestors of Neotropical migratory tyrannids
and other birds of tropical origin likely evolved migrationin tandem with gradual range expansion (via dispersal, notmigration) into the more-seasonal areas of North America.
Alternatively, some tropical species may have expanded
their ranges into North America prior to the increases inseasonality in the Miocene, and only those that evolved
migration in situ, like Emberizoidea, persisted. Althoughdistinguishing these two historical biogeographic scenarios
may not be possible in all cases, the selective forces acting
on birds of high-latitude origin to migrate are likely thesame as those that acted on birds of tropical origin thathave colonized high latitudes (Bruderer & Salewski, 2008):
escape from unfavourable seasonal conditions, coupled withselection for breeding-site fidelity, as an adaptive strategy for
persistence in a seasonal environment.
(2) Dispersal, tropical niche conservatism and thecolonization of seasonal environments
Seasonality is an environmental filter for persistence inthe temperate zone (Schluter, 2016), and the evolution of
migration is similar to other adaptations (such as freeze
tolerance in plants or hibernation in mammals) in allowing
certain lineages, but not others, to colonize or persist
at high latitudes. The pervasiveness of migration as an
adaptation to seasonality across the avian tree of life relative
to other adaptive strategies means that understanding global
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746
patterns of avian biogeography is not possible without anunderstanding of how and why migration evolves. However,whereas other adaptations to high-latitude life such as freeze
tolerance or hibernation result in a broadening of climaticniches, the use of migration as a persistence strategy results
in relative conservation of the thermal niche throughout
the year because migrants escape the harshest climates(Laube, Graham & Böhning-Gaese, 2015; Gómez et al.,2016; Eyres et al., 2017; Zurell et al., 2018; Somveille, Manica& Rodrigues, 2018a). Consequently, seasonal migration has
facilitated the colonization of several avian lineages of likely
tropical origin in the temperate zone (such as Tyrannidae) as
well as the persistence of high-latitude lineages as global
temperatures have cooled over time, such as Parulidae(Winger et al., 2012, 2014), without necessitating the dramatic
expansion of thermal tolerances required for adaptation to
year-round temperate conditions.
In other avian lineages that have not colonized highly
seasonal latitudes, the lack of a migratory response to seasonality may contribute to restricted tropical distributions.
For example, some large avian lineages, such as the antbirds(Thamnophilidae and Formicariidae), are fully tropical andalmost exclusively sedentary, despite high variation among
species in elevational distribution and ecology within thetropics (Krabbe & Schulenberg, 2003; Zimmer & Isler,
2003). Such restricted latitudinal distributions are typicallyexplained by greater niche conservatism relative to temperate species, which is a product of numerous factors including
dispersal ability and physiological adaptation (Janzen, 1967;
Wiens & Donoghue, 2004; Smith et al., 2012). But given thatseasonal migration, not cold tolerance, is the most widespread
adaption to high seasonality in birds, we must consider the
possibility that antbirds have failed to colonize temperate
latitudes not only due to low vagility (e.g. Moore et al., 2008),
propensity for invading new habitats or adapting physiologically to cold, but also due to a concomitant failure to evolvemigration at the more seasonal peripheries of their ranges.
That is, the lack of a migratory response to seasonality insome taxa may result in low survival and fitness of dispersers
at the edge of the range and dampen the opportunity for further dispersal and range expansion into seasonal areas. Only
two antbird species are thought to make regular seasonal
movements, with both of these species migrating locally at
the southernmost edges of their ranges in northern Argentina
in austral winter (Zimmer & Isler, 2003). This suggests thata migratory response to seasonality is not impossible in thisspeciose group, but highly unusual, and may contribute to
the restriction of geographic ranges to low latitudes.
Our suggestion that the absence of a migratory response
could restrict range expansion highlights the complex relationship between migration and dispersal. Because theevolution of migration via range expansion into a seasonal environment must first involve dispersal into a newenvironment, species with traits conferring higher dispersal
ability or propensity may be more likely to evolve seasonal
migration by virtue of greater exposure to selective pressures
to migrate. Additionally, there may be a correlation between
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Benjamin M. Winger and others
traits that mediate dispersal into new environments and thosethat enable an escape response to seasonally deteriorating
conditions, such as vagility (Salewski & Bruderer, 2007). Thatis, species that evolve migration may be those that not only are
more likely to disperse, including into seasonal environments,
but also are most likely to use escape as a persistence strategy
when seasonal conditions become inadequate. Therefore, thetraits identified as ‘evolutionary precursors’ (Levey & Stiles,
1992) to migration in tropical birds, such as use of open oredge habitats (e.g. Chesser & Levey, 1998; Outlaw & Voelker,
2006; Boyle & Conway, 2007; Bell, 2011), are not necessarily
unrelated to the evolution of migration. Rather, any relationship between, for example, habitat occupancy and migratory
versus sedentary behaviour is likely mediated by the intermediate influence of habitat on the propensity to disperse into
seasonal environments where selection pressures to evolvemigration are greater. Yet, the degree to which seasonal
migration promotes versus restricts dispersal behaviour at different spatial scales, and the influence of this relationshipon range expansion, is poorly understood and requires further research (Böhning-Gaese, González-Guzmán & Brown,
1998; Bensch, 1999; Hansson et al., 2002; Winkler, 2005;
Henningsson & Alerstam, 2008; Toews, 2017)(3) The evolution and persistence of disjunctgeographic ranges in long-distance migrants
Although many fascinating details of intraspecific variationin short-distance migratory behaviour demand investigation(Boyle, 2008; Boyle et al., 2010; Chapman et al., 2011; Zúñiga
et al., 2017), it is not difficult to understand the adaptive valueof short-distance migration in general terms. For example,
the migration of the White-throated Sparrow (Zonotrichia
albicollis) can be understood as a response to inadequate
resources in most of the breeding range during the winter,with a fitness advantage conferred to individuals that travel ashort distance south (Fig. 2). By contrast, in long-distancemigratory species, most fundamental aspects of ecology
and biogeography remain truly enigmatic. Why does theBristle-thighed Curlew (Numenius tahitiensis) breed only intundra on the north slope of Alaska and winter only onbeaches in the south Pacific (Marks et al., 2002)? Why
do Blackpoll Warblers, which prefer stunted boreal taiga
for breeding, undergo a phenomenally long and arduous
migration over the Atlantic Ocean to their wintering areas
in lowland Amazonia and forego breeding or winteringin every habitat in between (Fig. 2; Deluca et al., 2015)?
Although it is clear that migratory species are, as a general
pattern, tracking resources during their migrations (Eyres
et al., 2017; Zurell et al., 2018; Somveille et al., 2018a), thedetails of species’ distributions remain difficult to understand:ecological idiosyncrasies and bizarre range disjunctions are
the norm rather than the exception among long-distancemigratory species.
Conceptualizing migration as a strategy for persistence
in a seasonal environment driven by fidelity to breedingsites removes the mystery, if not the idiosyncrasy, of disjunctbreeding and winter ranges in long-distance migratory

The evolution of seasonal migration
species. Present-day winter ranges are simply the locations
that have allowed individuals to maintain reproductive success on the breeding grounds. Severe disjunctions between
breeding and winter ranges in long-distance migratory
species have likely evolved gradually and reflect the dynamic
and stochastic nature of range evolution. For example, as
breeding ranges at high latitudes contracted, expanded andshifted during cycles of glaciation (Milá, Smith & Wayne,2006), so too have winter ranges and migratory routes – andfield studies of small-scale range shifts over recent decades,such as in Icelandic Black-tailed Godwits, suggest themechanism for both breeding- and winter-range shifts is
natal dispersal (i.e. population recruitment; Gunnarsson
et al., 2005, 2006). Over millennia, however, winter ranges inmore climatically stable lower latitudes may not have shifted
as much as high-latitude breeding ranges as a consequence ofglaciation cycles, potentially resulting in the poleward shifting of breeding ranges while the location of the winter range
has remained relatively more static (Ruegg & Smith, 2002;
Milá et al., 2006; Zink & Gardner, 2017). Consequently,
the perplexingly long-distance migratory journeys that so
capture our imagination, such as the Bristle-thighed Curlew
or the Blackpoll Warbler, reflect the ‘whatever works’ natureof migration as a persistence strategy: because migratory
behaviour is highly heritable either genetically or culturally,
winter ranges and extreme migratory routes may persist
through generations (and perhaps millennia) as long as they
confer sufficient over-winter fitness to maintain reproductive
success the following breeding season (Conklin et al., 2017).
The paired association of breeding and winter ranges
among migratory populations are further idiosyncratic asa consequence of phylogenetic diversification. Assuming a
non-sympatric speciation model, speciation in migratory
lineages necessarily involves cladogenic inheritance of only aportion of the breeding range (Ree et al., 2005). Dependingon patterns of migratory connectivity (see Section VI),
cladogenesis likely involves inheritance of only a portion of
the wintering range as well, resulting in daughter species
with idiosyncratically divided breeding and winter ranges(Winker & Pruett, 2006; Ruegg, 2008; Winker, 2010;
Winger et al., 2012, 2014).
Our suggestion that historical stochasticity underlies muchof the idiosyncrasy of long-distance migration does not
imply that ecological adaptations to specific winter areas bylong-distance migrants are unimportant. On the contrary,full-annual-cycle studies of migratory populations reveal
that, within species, the nuances of winter ecology arehighly consequential for reproductive success in subsequent
breeding seasons (Norris et al., 2004; Reudink et al., 2009;
Marra et al., 2015; Rushing et al., 2015). Collectively, thesestudies suggest that expansion of or changes to winterranges in long-distance migrants is not simply a matterof achieving over-winter survival or improving wintercondition of migratory individuals, which could lead to highlability of the winter range at the species level. Rather, forgeographic modifications of non-breeding ranges to persist,changes in winter distributions or ecology must translate

747
to higher reproductive success than conspecifics (Bearhop
et al., 2005) or new migratory strategies will not proliferate
in a population. The intricate relationship between winterecology and breeding success may therefore confer a measureof temporal stability to migratory patterns in some species,
resulting in the persistence of long-distance migrations evenwhen closer suitable winter ranges or more efficient migratoryroutes (e.g. Somveille et al., 2018a) are theoretically available.
However, stability and persistence of migration is notconsidered the norm. Rather, the dominant viewpoint on
the evolution of migration is one of high lability andplasticity. Because migration has been shown to evolve
rapidly in some species, it is often stated that migratory
behaviour is universally labile (e.g. Helbig, 2003; Pulido,2007). Most evidence for rapid changes in migration comefrom a small number of species of facultative or partial
migrants, most prominently the Eurasian Blackcap (Sylvia
atricapilla), a species which exhibits substantial diversity
in migratory behaviour and has modified its wintering
range in recent decades (Berthold et al., 1992; Pulido &Berthold, 2010). The variability in migration displayed by
the Eurasian Blackcap provides an excellent system forresearching many aspects of the evolution of migration(Pulido, 2007), but how conclusions drawn from researchon partial or facultative migrants should be applied tomigratory species more broadly requires critical thought(Piersma et al., 2005; Piersma, 2011). In particular, it isimportant to recognize that the role of plasticity in evolution
is not only a story of the maintenance of plasticity andconstant fluidity in trait evolution, it is also frequently a storyof the loss of plasticity due to genetic assimilation (Price,
Qvarnstrom & Irwin, 2003; West-Eberhard, 2003; Pigliucci,
Murren & Schlichting, 2006). During genetic assimilation,changes in the environment expose plastic phenotypes tostrong selection, potentially towards new adaptive peaks. If
shifts in environmental conditions are persistent throughout
generations, plasticity may be lost and phenotype will nolonger vary according to previous reaction norms. Thatis, selection for a particular extreme of an initially plastic
phenotype can result in the loss of plasticity.
Canalization of migratory traits (i.e. loss of plasticity) likely
plays an underappreciated role in the evolution of migratory
patterns (Winker, 2010; Pulido, 2011). In particular, theidiosyncratic ranges and routes of obligate long-distancemigratory species may be evidence of canalization ofplasticity in migratory behaviour in conjunction withstochastic biogeographic changes. Therefore, the fluidityof migratory behaviour in some species is not evidence
that migration in all lineages is subject to rapid change.
Rather, it is evidence that migration is a behaviourally
plastic trait – and behaviourally plastic traits may be subject
to genetic assimilation and the loss of plasticity (Ehrenreich& Pfennig, 2016). Thus, in some species, obligate migratory
behaviour may have persisted even as geographic ranges
shifted (for example, during glacial cycles, which haverecently been regarded as implicitly necessitating profoundshifts in migratory behaviour; Zink & Gardner, 2017). In
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748
other species in which plasticity for migration persists or isitself adaptive, subtle environmental changes may lead to
rapid changes in a population’s migratory behaviour due tosensitivity to variation in reaction norms; such plasticity
likely accounts for changes to the migratory behaviour
and geographic range observed in some species over years
or decades (e.g. Able & Belthoff, 1998). Across species,
variability in the maintenance of plasticity for migratory
traits versus their past canalization and loss of plasticity
may underlie much of the fascinating idiosyncrasy anddiversity observed in species’ migratory routes and ranges
and will likely influence their adaptive responses to rapid
anthropogenic climate change (Gilroy et al., 2016; Senner,
Stager & Cheviron, 2017; Williams et al., 2017).

VI. SYNOPSIS: A LONG WINTER FOR THE RED
QUEEN
The Lewis Carroll quote that inspired Van Valen’s (1973)
Red Queen hypothesis for persistence in a changing
environment (‘it takes all the running you can do, to keepin the same place’) has illuminated numerous evolutionary
phenomena related to the ever-shifting nature of adaptation.
If readers will indulge a more literal interpretation of
the metaphor than intended by Van Valen, the Red
Queen’s axiom also provides a succinct summary of our
synthesis of the evolution of seasonal migration. Organisms
increase their reproductive success through breeding-site
fidelity, that is, staying in or near to the same place.
In environments in which resources seasonally become
scarce and environments harsh, organisms must evolve
adaptations to these cyclical environmental changes toachieve the reproductive advantages associated with site
fidelity. Some organisms evolve physiological, neurological or
behavioural adaptations that keep them near their breedingareas through the harshest times of year; but in many
bird species, migrating has proven the most successful
solution. It takes all the flying you can do to keep in thesame place.
A central question for understanding the evolution of
migration, then, is why is there such tremendous variationin migratory journeys even among species that breedin similar locations? Migratory distance varies markedly
among closely related species, and also among individualsof some populations, making it difficult to understand why
specific migratory strategies or routes have evolved. Hermit
Thrushes (Catharus guttatus), Swainson’s Thrushes (C. ustulatus)
and Veeries (C. fuscescens), three closely related species,
frequently breed in the same hectare of eastern North
American temperate forest but winter in drastically different
regions – one in the southern USA, one in the Andes, andthe other in Amazonia (Outlaw et al., 2003). We know agreat deal about the natural history of these three species
and have learned much about how they accomplish theirmigrations (e.g. Bowlin & Wikelski, 2008; Deppe et al., 2015;
Gómez et al., 2017), but we have few answers as to why the
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Benjamin M. Winger and others
migratory journeys and strategies of these species differ fromone another, other than to dismiss the question outright byacknowledging that all geographic ranges are idiosyncraticand ephemeral reflections of numerous biotic, abiotic andhistorical factors.
Over the last two decades, many studies have begun
leveraging technological advantages to study the relationshipbetween breeding and winter locations within migratory
species (Rubenstein et al., 2002; Webster et al., 2002; Cohenet al., 2017). This is the field of migratory connectivity, whichseeks to describe how the location where an individual breeds(in the context of the full breeding range of its species) predicts
the spatial location of its wintering location (within the winterrange of its species). Collectively, these studies have revealed
much idiosyncrasy in connectivity among species (Cohenet al., 2017). For example, some species exhibit parallel,
and thus somewhat predictable connectivity, with eastern
breeders wintering east of western breeders throughout theirranges (Kramer et al., 2018), whereas other species havemore surprising crosswise migrations between breeding andwintering locations (Witynski & Bonter, 2018).
Given such idiosyncrasy in migratory connectivity within
species, it is natural to focus on individual-level variation in
migratory behaviour, and indeed this variation has important
implications for the ecology and conservation of migratory
birds (Cooper et al., 2018; Kramer et al., 2018). However, thegeographic ranges of species are emergent properties of the
movements and territories of individuals. As the connectivityof more species is described, the synthesis of this information
across species will provide a yet-untapped potential tounderstand the evolution of broader biogeographic patterns.
For example, to what extent do migratory species trackcertain habitat requirements, as opposed to climaticconditions, making distributions ecologically deterministic(Thorup et al., 2017)? How does competition among closely
related species vary throughout the annual cycle and dictateseasonal patterns of sympatry versus segregation (Gross& Price, 2000)? By continuing to gather natural-history
information on species’ migratory behaviour and contextualizing this variation as alternative manifestations of an
adaptation that enables species to persist in fluctuating andever-changing environments, migratory species will provide
a powerful lens into the factors that control local adaptationand geographic range evolution as well as species’ ability topersist in our present rapidly changing world.

VII. CONCLUSIONS(1) Understanding the evolution of migration and its
consequences for geographic range dynamics has been
constrained by the assumption that migration arose as ameans of colonizing new breeding sites in regions that were
thought to confer higher reproductive success.
(2) We argue that migration has evolved following regular(i.e. short-distance) breeding dispersal into seasonal areas orfollowing increases in seasonality within existing ranges, asThe evolution of seasonal migration
an adaption for persistence analogous to other strategies forcoping with fluctuating environments.
(3) We propose that the reproductive benefit ofmaintaining fidelity to breeding sites has selected for regular,
cyclical migrations in many species as opposed to nomadic
behaviour or irregular movements. That is, returning tofamiliar locations for breeding, as opposed to exploringnew sites for breeding, underlies the evolution of seasonal
migration as a strategy to persist in seasonal environments.
This hypothesis is supported by decades of research on
the breeding biology of migratory birds, as well as theory
suggesting that species prefer their natal habitats when
undergoing dispersal. The adaptive value of migrating long
distances to maintain site fidelity can be conceptualized as abiogeographic Red Queen metaphor.
(4) Regarding seasonal migration as an adaptation thatfacilitates persistence in seasonal environments allows thedecoupling of the biogeographic origins of migratory lineages
and the mechanism by which migration evolves. Thus,
lineages may be of broadly different biogeographic origins(e.g. Southern versus Northern Hemisphere) but neverthelessevolve migration in seasonal environments as a consequenceof the same selection pressures to cope with seasonality.
This decoupling of history and mechanism will lead to amore productive analysis of geographic range evolution in
lineages containing migratory species and the mechanisms
by which disjunct wintering and breeding ranges arise andare maintained through time.
(5) Our conceptualization of the evolution of migration
places new emphasis on previously under-appreciatedavenues of research. In particular, understanding theevolutionary trade-offs of adopting migration as opposed toalternative coping strategies for seasonal resource limitationand harsh environmental conditions is an underexploredarea of research in organismal biology.
(6) Geographic ranges are fluid and complex phenomena,even in sessile species, and ranges are sometimes thought
to be even more mutable in migratory species due tothe rapidity with which migratory behaviour can change.
However, the role of genetic assimilation (i.e. loss ofplasticity) in the evolution of migratory patterns has been
under-appreciated and may help explain the idiosyncratic
migratory routes and distributions observed in many
species.
(7) An improved understanding and contextualizationof the ecological and historical linkages between breeding
and non-breeding locations within migratory species will
provide a promising framework from which to illuminate
the forces that dictate where and when species exist acrossthe earth.

VIII. ACKNOWLEDGMENTS
For helpful comments on the manuscript we thank Eric
Gulson-Castillo, Benjamin Van Doren, and two anonymous
reviewers.

749
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(Received 8 June 2018; revised 2 October 2018; accepted 8 October 2018; published online 4 November 2018)

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