Introduction
Seasonal migration is common in nature
(Dingle, 2014) and allows many different
animals to escape deteriorating habitats, escape predators and
parasites, and benefit from seasonally available resources in multiple
regions (Dingle, 1972;
Alerstam, Hedenstrom & Åkesson, 2003;
Alerstam, 2006;
McKinnon et al. , 2010;
Altizer, Bartel & Han, 2011;
Fricke, Hencecroth & Hoerner, 2011;
Dingle, 2014). Migration is likely to be
polygenic (Dingle, 1991) and studies have
demonstrated that genes involved in muscle development, energy
metabolism and circadian rhythm tend to show genetic divergence or
differential expression patterns between migratory and non-migratory
individuals (McFarlan, Bonen & Guglielmo,
2009; O’Malley, Ford & Hard, 2010;
Postel, Thompson, Barker, Viney & Morris,
2010; Trivedi, Kumar, Rani & Kumar,
2014). While it is clear that migration imposes selection for specific
gene variants or transcription levels, the interplay between animal
migration and genome evolution remain understudied. Genomes may be
affected by migration in varying ways. Populations of the same species
often vary in their migratory propensity, with some populations
migrating and others not, or with populations migrating over different
distances and to different destinations. This could result in spatial or
temporal separation between different migrants, and consequently reduced
gene flow and increased genome-wide genetic differentiation, as found in
beluga whales and noctule bats
(O’Corry-Crowe, Suydam, Rosenberg, Frost
& Dizon, 1997; Petit & Mayer, 2000).
Alternatively, the use of common breeding or overwintering grounds can
result in a lack of genome-wide differentiation, even if differential
selection acts on individuals during part of the year
(Dallimer & Jones, 2002;
Dallimer, Jones, Pemberton & Cheke,
2003). An extreme example occurs in Pacific salmon, in which the
genetic differentiation between early (premature) and late (typical,
mature) migrants is restricted to a single gene, GREB1L(Prince et al. , 2017); while
selection acts on this gene seasonally, large amounts of gene flow
homogenize the remainder of the genome. Insights into the genetic basis
of animal migration thus require genome-wide studies, to identify genes
that are under selection against a potential background of variable gene
flow (Bensch, Andersson & Åkesson, 1999;
Liedvogel, Åkesson & Bensch, 2011).
Eastern North American monarch butterflies undergo one of the most
well-known and spectacular migrations of the animal kingdom
(Gustafsson, Agrawal, Lewenstein & Wolf,
2015; Reppert & de Roode, 2018), with
up to hundreds of millions of butterflies migrating up to 4,500 km to
reach their overwintering sites in central Mexico
(Urquhart & Urquhart, 1978;
Brower, 1995;
Flockhart et al. , 2017). Monarch
caterpillars are specialist feeders of milkweed host plants, which die
back seasonally in North America, thereby preventing monarchs from
breeding throughout the year. In the fall, developing monarch
caterpillars respond to changing temperature, shortening day length and
senescing host plants to enter a state of reproductive diapause
(Goehring & Oberhauser, 2002), which
enables them to survive the 6-8 months that it takes to migrate south,
overwinter, and re-migrate north in the spring
(Herman & Tatar, 2001). Prior to spring
re-migration, overwintering monarchs complete reproductive development
and mate at the Mexican overwintering sites or in their recolonized
breeding areas (Herman, Brower & Calvert,
1989). Monarchs recolonize the southern parts of the United States and
lay eggs on re-emerging milkweed, and 2-4 successive generations of
reproductive monarchs recolonize their entire 4.5 million
km2 breeding range
(Flockhart et al. , 2013).
While monarchs are best known for this long-distance migration from
eastern North America to Mexico, monarchs that inhabit breeding grounds
west of the Rocky Mountains migrate shorter distances to overwinter in
groves of Eucalyptus and native conifers along California’s Pacific
Coast (Nagano et al. , 1993;
James et al. , 2018). Whereas
eastern monarchs may fly over 4,500km to reach the Mexican overwintering
sites, western monarchs reach the California Coast by flying as little
as 500km, with the greatest recorded distances being 1,600km
(Yang, Ostrovsky, Rogers & Welker,
2016). Whether these dramatic differences in migration distance are the
result of differential selection, or plasticity from genotype by
environment interaction remains unknown. Eastern and western North
American butterflies have divergent wing morphology
(Altizer & Davis, 2010;
Freedman & Dingle, 2018), and it is
often assumed that they form distinct genetic populations
(Brower et al. , 1995;
NatureServe, 2019). However,
observational studies (Brower & Pyle,
2004) and limited allozyme and microsatellite studies
(Shephard, Hughes & Zalucki, 2002;
Lyons et al. , 2012) have indicated
large amounts of genetic exchange between eastern and western monarchs.
This lack of genome-wide genetic differentiation suggests that migratory
differences may instead be driven by restricted loci or differential
environment-induced gene expression
(Liedvogel et al. , 2011). Here, we
compare flight performance of eastern and western monarchs, carry out an
analysis of 43 genomes (Fig. 1), and measure the expression of a small
number of candidate genes in eastern and western monarchs during flight
trials.