DISCUSSION
In the present study, we investigated the genetic architecture of
dispersal in an insular metapopulation of house sparrows by estimating
additive genetic and environmental variance components complemented by a
genome-wide association analysis. Our house sparrow metapopulation is
particularly interesting for such a study, as previous publications have
shown that birds differ in dispersal probability depending on whether
they originate from a farm or non-farm habitat type of island (Pärn,
Ringsby, Jensen, & Sæther, 2012; Ranke et al., 2021; Saatoglu et al.,
2021). We found that in this metapopulation, heritable genetic variation
explained approximately 10% of the variation in individual dispersal
probability. However, by using novel statistical methods that allow for
mean and variance in heritable genetic variation to differ between
genetic groups, we revealed that the farm and non-farm habitats differ
in both mean breeding values and additive genetic variances for
dispersal. Specifically, although phenotypic dispersal probabilities are
higher in the non-farm habitat, the mean breeding value and the additive
genetic variance (as well as the heritability) for dispersal was higher
in the farm habitat than in the non-farm habitat.
It is challenging to obtain high quality data on dispersal because the
study system needs to be sufficiently large to cover normal dispersal
distances of the organisms, resident and dispersing individuals need to
be individually recognizable, and to estimate either the heritable
genetic component of dispersal or its fitness consequences,
cross-generational data that include information also on the descendants
of dispersers and residents are necessary (Cayuela et al., 2018;
Holyoak, Casagrandi, Nathan, Revilla, & Spiegel, 2008; Millon, Lambin,
Devillard, & Schaub, 2019). Despite these challenges, the genetic basis
of dispersal phenotype and dispersal-related traits had been researched
on occasion even in vertebrates in the wild, using either
parent-offspring regressions or animal models. Parameter estimates
derived from animal models, which account for all kinds of genetic
relatives in the models and are regarded as potentially less biased by
for example non-genetic environment effects than parent-offspring
regressions (Kruuk, Slate, & Wilson, 2008), tend to report more modest
magnitudes of σA2 andh2 than parent-offspring regressions
(Saastamoinen et al., 2018). Furthermore, animal model-based heritable
genetic parameters of dispersal propensity for Aves class members of
natural populations were reported as 0.024 – 7.608 and 0.36 – 0.95 forσA2 andh2 , respectively (Supplementary Table S3).
Moreover, the σA2 andh2 of dispersal were estimated to be 0.290 and
0.280, respectively, in an experimental cane toad study (Bufo
marinus/Rhinella marina ; Phillips, Brown, & Shine, 2010), and in a
semi-natural common lizards (Zootoca vivipara ) study as 1.148 and
0.170, respectively (San‐Jose et al., 2023). Hence, heritability
estimates of dispersal for other species are usually higher than those
we documented in house sparrows, although our estimate ofσA2 for the farm habitat was
slightly higher than in the metapopulation as a whole, with
approximately 12% of the phenotypic variance in dispersal explained by
heritable genetic variation in this habitat type (Table 1). In
combination, the relatively few studies on the heritable genetic basis
for dispersal propensity that exist from natural vertebrate populations
(Supplementary Table S3) suggest that this key life-history trait has
the capacity for adaptive evolution on ecological time-scales if any
selection is acting on it, but that its rate of micro-evolution may
differ somewhat between species and even between populations within the
same species. Indeed, in another study of the same house sparrow
metapopulation we have shown that immigrants have higher fitness than
resident individuals (as estimated by annual production of recruiting
offspring and number of recruiting offspring produced over the life
span; Saatoglu et al., in preparation). Consequently, dispersal rates
are expected to increase across generations in our metapopulation.
Recently, gene mapping studies using a GWAS approach have been able to
identify genes underlying phenotypic variation in various heritable
life-history and fitness-related traits even in natural vertebrate
populations (e.g. Barson et al., 2015; Husby et al., 2015; Johnston et
al., 2011; Lawson & Petren, 2017; Lundregan et al., 2018; Tietgen et
al., 2021). Here, we have revealed a single region on chromosome 15 that
was linked with dispersal trait in the house sparrow metapopulation and
it has been found that this marker was closest to the ADORA2A receptor
gene. This receptor gene is located near the UPB1 gene both in the house
sparrow genome (Elgvin et al., 2017) and the zebra finch genome (Warren
et al., 2010). ADORA2A is involved in glycogenolysis (i.e. release of
the glucose into the bloodstream; see González-Benítez et al., 2002),
thus ADORA2A may influence energy dynamics. Glucose metabolism has been
shown to affect dispersal rate in the Glanville fritillary butterfly
(Melitaea cinxia) for which the Pgi gene explains
variation in dispersal rate, and is involved in breakdown of glucose to
produce ATP (Hanski et al., 2017; Niitepõld & Saastamoinen, 2017).
Interestingly, another function of ADORA2A is to increase intracellular
cAMP levels which are not only important in metabolism and wakefulness
but are also an important aspect of the circadian regulatory mechanism
that has direct influence on the clock phase (O’Neill & Reddy, 2012). A
recent study on a semi-natural population of common lizards
(Zootoca vivipara ) showed that expression of circadian clock
genes differed between dispersers and residents. However, ADORA2A or
UPB1 were not among the dispersal-related genes identified in these
species (San‐Jose et al., 2023). Moreover, clock-linked genes may also
influence migratory timing in the American kestrel (Falco
sparverius ; Bossu, Heath, Kaltenecker, Helm, & Ruegg, 2022). Hence,
although few studies exist and the functional relationship between
putative genes and dispersal in most cases needs to be explored further,
there appears to be some evidence that genes related to (flight) energy
metabolism and circadian rhythms are related to the individual dispersal
processes. However, it seems clear that dispersal propensity at least in
our house sparrow metapopulation is a polygenic trait with a complex
basis that involves both genes and environmental effects.
Dispersal in our house sparrow metapopulation occurs during the fledged
juvenile phase, in the autumn before the juveniles’ first winter (Pärn,
Jensen, Ringsby, & Sæther, 2009; Ranke et al., 2021; Saatoglu et al.,
2021). Thus, it seems likely that environmental conditions related to
the population density, weather or various habitat characteristics that
offspring experience during development may also affect the propensity
to disperse. Accordingly, we have previously shown in the same study
system that dispersal rates were higher when springs were warmer,
breeding started early, and when total population sizes at the end of
the breeding season were higher (Pärn et al., 2012). Condition-dependent
dispersal probabilities that are influenced by environmental conditions
such as population density, prenatal/postnatal environmental conditions
and/or physiological traits underlying the movement capacity have also
been documented in many other studies of vertebrates (Boualit et al.,
2019; Leon, Banks, Beck, & Heinsohn, 2022; Maag, Cozzi, Clutton-Brock,
& Ozgul, 2018; Massot, Clobert, Lorenzon, & Rossi, 2002; Matthysen,
2005; McCaslin, Caughlin, & Heath, 2020; Messier, Garant, Bergeron, &
Réale, 2012; Saastamoinen et al., 2018; Walls, Kenward, & Holloway,
2005; Wu & Seebacher, 2022). Interestingly, the relationships between
dispersal and environmental conditions in our house sparrow
metapopulation mentioned above actually differed between habitat types:
dispersal rates were positively related to spring temperature, onset of
breeding and total population density in non-farm habitat islands, while
dispersal was independent of these environmental conditions in farm
habitat islands (Pärn et al., 2012). Despite higher average dispersal
rates in the non-farm habitat than in the farm habitat (Ranke et al.,
2021; Saatoglu et al., 2021), the results in the current study that show
lower estimated mean breeding values and lower additive genetic
variances for dispersal in the non-farm habitat than the farm habitat
(Table 1), suggest that when individuals make their dispersal decisions,
environmental components are more influential than heritable genetic
effects in the non-farm habitat.
Moreover, the contrasting results for the two habitat types such as
lower mean breeding values but higher dispersal probabilities in the
non-farm habitat type and differences between islands within each
habitat type in dispersal probabilities (Supplementary Figure S3)
suggest that there may be a genotype by environment interaction
(GxE ) for dispersal in our house sparrow metapopulation. If such
an interaction exists, one would expect that birds with genomes
originating from non-farm islands will respond differently to the farm
environment with respect to their dispersal probabilities and vice
versa. Birds that disperse between habitat types and the descendants of
such inter-habitat dispersers (see Supplementary Figure S1) can not only
be used to separate additive genetic effects from environmental causes
of observed differences in dispersal probabilities such as we have done
here (Table 1; Figure 3), they also allow for examining GxE in
dispersal. Testing whether there is a GxE for dispersal in our
study metapopulation, and investigating any causes and consequences of
such an interaction is however outside the scope of the current paper
and should be examined in a future study.
Here we have shown that there is a habitat-dependent heritable basis for
dispersal, which is an important life history trait because of its close
connection with spatio-temporal ecological and evolutionary and dynamics
across geographically structured populations (Clobert et al., 2012;
Saastamoinen et al., 2018). The ability of evolutionary ecologists to
partition a natural population’s phenotypic variance in key traits into
a heritable genetic component and environmental components of variation
advanced when animal models were introduced to the field approximately
two decades ago (Kruuk, 2004; Wilson et al., 2010). Here we have
exploited the recent development of genetic groups animal models that
allow for exploring and quantifying spatial variation in heritable
genetic variation (Aase et al., 2022; Muff et al., 2019) and show that
the rate of any adaptive evolutionary change in dispersal may differ
across space in a fragmented population. In a rapidly changing world,
where many populations become increasingly fragmented and range shifts
may be necessary to avoid extinction, quantifying such spatial variation
and understanding its consequences for ecological and evolutionary
processes is likely to be of increasing importance.