Morphological analyses
To analyze the effect of time on body measurements, we measured 87
individuals, 55 males and 32 females. We used principal component
analysis (PCA) using “FactoMineR” to condense the six body
measurements into two variables with eigenvalues > 1, which
together explained 60% of the total variance. The first principal
component (PC1) correlated with tarsus length, tail length, wing chord
length, and beak depth; the second principal component (PC2) correlated
with exposed culmen length and beak width (Table 2). We performed a
generalized linear mixed models (GLMMs) with a gamma error distribution,
using “lme4”. In these analyses we included populations (MTV, HDA,
UCR, and JBL), time periods (period 1 and period 2) and the interactions
between both variables, as independent variables; each of the two
principal components (PC1 and PC2) as the response variable, and the
territory inside each population in which individuals were captured as
random factor. We also performed models for females and males because
males are larger than females (Sandoval & Mennill, 2013). We carried
out post hoc tests when the model showed significant differences on
pairwise comparisons between the main effects and the two-factor
interactions.
Finally, to evaluate if divergence between different traits (i.e.,
genetic, acoustic, and morphology) is related, we conducted a partial
Mantel test to determine the strength of the correlation between
variables using 10,000 permutations implemented in the “vegan” package
in R (Oksanen et al., 2012). Females in this analysis were not
considered because they do not sing (Sandoval and Mennill 2014; Sandoval
et al. 2016). We used 46 males with data of the three variables. First,
we performed a PCA to condense the six body measurements and another PCA
to condense the five song measurements of the males. With the PCAs we
then obtained acoustic and morphological distance matrices created from
Euclidean distances of averaged population traits in time periods, and
the genetic distance matrix from Gst values.
Results
Genetic diversity
At UCR, observed heterozygosity (\(H_{o}\)) was greater in ’period 1’
than in ’period 2’ (z = 1.95, p = 0.05), whereas the genetic diversity
of the other populations did not differ between time periods (all
comparisons: z 1.01, p > 0.05) (Table 3). In Heredia,
period 1 had a lower expected heterozygosity (\(H_{e}\)) than period 2
(z = -2.37, p < 0.05). In contrast, heterozygosity was lower
in ’period 1’ for the JBL population than in ’period 2’ (z = -2.37, p
< 0.05), whereas the other populations did not differ (all
comparisons: z = 0.68, p > 0.05) (Table 3). HDA, JBL, and
UCR showed significant inbreeding in ’period 2’ (Table 3).
Genetic diversity was significantly structured in the metapopulation;
however, structure did not differ between time periods: period 1
(\(G_{\text{st}}\) = 0.07, 95% CI = 0.06 and 0.09) and period 2
(\(G_{\text{st}}\) = 0.07, 95% CI = 0.06 and 0.09). AMOVA results
showed that 12% of total genetic variation was partition among
individuals in different time periods. There were significant
differences in allele frequencies between periods (i.e., period 1 vs.
period 2; \(F_{\text{ct}}\) = 0.120, p < 0.05), as well as
among populations within time periods (\(F_{\text{sc}}\) = 0.15, p
< 0.001). In both time periods, the Evanno method suggested
that populations were likely grouped into two clusters (i.e., K=2). In
‘period 1’, all MTV individuals were assigned to cluster 1, while nearly
all HDA, UCR, and JBL individuals were assigned to cluster 2 (Figure 1).
In ‘period 2’ individuals were also grouped into K = 2 clusters, with
individuals from MTV grouped in cluster 1, and the individuals from the
other populations were almost equally distributed into clusters 1 and 2
(Figure 1).
Acoustic characteristics of songs
We found that the duration and number of elements (PC1) were affected by
the time period and by the interaction between population and time
period (Table 4). In MTV, songs increased in duration and number of
elements in ‘period 2’ (Figure 2). The minimum and maximum frequency
(PC2) were not affected by time, but it differed significantly among
populations (Table 4). UCR had higher minimum frequency and lower
maximum frequency than MTV and HDA; while JBL had lower minimum
frequency and higher maximum frequency compared to other populations
(Figure 2). The frequency of maximum amplitude (PC3) showed significant
differences in the interaction population × time period (Table 4). The
songs increased the frequency of maximum amplitude in HDA period 2,
relative to ’period 1’, whereas UCR and JBL decreased in ’period 2’
compared to ’period 1’.
Morphology
We found a significant
interaction between population and time period in females
for tarsus length, tail length,
wing chord length, and beak depth (PC1) (Table 5). These morphological
variables represented by the PC1 decreased between periods 1 and 2 for
MTV and JBL (Figure 3). The exposed culmen length and beak width (PC2)
did not show significant differences (Table 5) among sites or time
periods. For males we also found a significant interaction between
population and time period for PC1 (Table 5). Tarsus length, tail
length, wing chord length, and beak depth were smaller in JBL period 2
compared to period 1 (Figure 3). The exposed culmen length and beak
width (PC2) were affected by the interaction between population and time
period (Table 5). Birds in MTV period 2 had shorter exposed culmen and
bigger beak width than in period 1, and birds in JBL period 2 had bigger
exposed culmen length and smaller beak width than in period 1 (Figure
3).
Relationship between variables
When acoustic differences were controlled, the partial Mantel test
revealed a non-significant association between genetic and morphological
distances (r = -0.06, p = 0.40; Figure 4). Similarly, we found no
significant correlation between morphology and acoustic distances, while
accounting for genetic differences (r = 0.24, p = 0.10; Figure 4).
However, we found a significant correlation between genetic distances
and acoustic distances when morphological distances were accounted for
(r = 0.49, p < 0.05; Figure 4).
Discussion
Our findings showed an increase in inbreeding, as well as changes in
acoustic and morphological traits over a ten-year period, however only
genetic distances and song divergence correlated. These results are
likely explained by the interaction between changes in habitat quality
and the barriers to gene flow produced by rapid urban development in the
sampling area (Biamonte et al., 2011; Rodríguez-Bardía et al., 2022).
Particularly considering the low mobility, isolation and specific
habitat requirements of white-eared ground-sparrow (Delaney et al.,
2010a; Rodríguez-Bardía et al., 2022; Soulé et al., 1988).
Genetics
We found an increase in inbreeding in three populations exposed to rapid
urbanization in the Costa Rican Central Valley (HDA, JBL, and UCR).
Inbreeding is caused by consanguineous mattings, and its extent is
proportional to a reduction in effective population sizes, or a
reduction in the dispersal of individuals among populations (Frankham et
al., 2002). Therefore, the increase in inbreeding could be explained by
urban expansion which rapidly transforms natural ecosystems into
homogenized environment that limits resources to small suboptimal
patches of vegetation (Biamonte et al., 2011; Fahrig & Rytwinski, 2009;
Miles et al., 2019). These drastic changes brought about by urbanization
restrict the movement of birds between populations (Rodríguez-Bardía et
al., 2022). Consequently, small and isolated populations increase the
likelihood of mating with relatives (Wright et al., 2008). A similar
increase in inbreeding associated with isolation and urban development
was reported for the european treefrogs Hyla arborea (Andersen et
al., 2004) and was also found in birds, the taita thrush Turdus
helleri (Lens et al., 2000).
Our analysis found that spatial genetic structure is more affected by
distance than by time. This result is consistent with the isolation by
distance and the urban resistance to gene flow previously reported for
this species (Rodríguez-Bardía et al., 2022). Additionally, this
condition is typical for species with low mobility and specific habitat
requirements, such as the white-eared ground-sparrow.(Delaney et al.,
2010b; Rodríguez-Bardía et al., 2022; Soulé et al., 1988). However, the
Bayesian clustering suggests that some movement of individuals may still
occur among populations. Therefore, our results suggest that we are
witnessing the progressive decline of gen flow and genetic diversity
over time.
The indirect evidence of limited gene flow found in our study, could be
also a result of the interaction between philopatry, territoriality and
the lack of suitable habitat for populations of ground-sparrows in an
urban setting. Philopatry and territoriality keep individuals within a
population, thereby decreasing gene flow and increasing genetic
differentiation between populations (Bounas et al., 2018;
Rodríguez-Bardía et al., 2022). In urbanized sites ground-sparrow males
may increase their territories to search for additional food sources
(Juárez et al., 2020). This foraging behavior could obligate males to
migrate when resources are scarce. Thus, this behavior could explain to
the movement of individuals showed in our Bayesian clustering.
On the contrary, individuals inhabiting isolated populations might
develop local adaptations, such as different dialects and variations in
the frequency and duration of songs, as shown for the white-eared
ground-sparrow (Sandoval et al., 2014, 2015, 2016; Juárez et al., 2020;
Méndez et al., 2021). These adaptations could further reduce individuals
dispersal between populations, thus contributing to increase genetic
differences among remaining populations (Morhina et al., 2017). For
example, in white-crowned sparrows Zonotrichia leucophrys , the
genetic structure was correlated with song dialects, because song
dialects act as barriers for migrant males, increasing genetic structure
of populations (MacDougall-Shackleton & MacDougall-Shackleton, 2001).
We only observed decline in genetic diversity in the population at the
most urbanized location (\(H_{\text{o\ }}\) UCR period 1: 0.62 vs\(H_{\text{o\ }}\) UCR period 2: 0.32). This result is consistent with
previous research indicating that urbanization reduces genetic diversity
in wren-tits Chamaea fasciata , side-blotched lizards Uta
stansburiana , western skinks Plestiodon skiltonianus , and
western fence lizards Sceloporus occidentalis inhabiting more
isolated habitat patches (Delaney et al., 2010b). Therefore, cities and
human-made structures are clearly acting as a barriers to gene flow
(Rodríguez-Bardía et al., 2022), that limits the movement of individuals
among vegetation remnants within cities. So, in the span of a decade we
were able to document a decrease in genetic diversity of this bird
species in the most urbanized populations. Due to the small number of
individuals captured at UCR during ‘period 2’ our findings must be
interpreted with caution.
Acoustics
Differences in solo songs of white-eared ground-sparrows are concordant
with previous studies which reported acoustic differences as a possible
adaptation to urban noise (Méndez et al., 2020; Sandoval et al., 2016;
Sandoval & Mennill, 2014; Bonilla-Badilla 2021). However, we
additionally discovered a correlation between acoustic and genetic
distances while controlling for morphology. These results reaffirmed the
urban development as an important barrier among populations, that
isolate and limit the movements of individuals (Rodríguez-Bardía et al.,
2022; Sosa-López et al., 2013). The same relationship between genetic
and acoustic distances has been reported in populations of rufous-naped
wren Campylorhynchus rufinucha which lost connectivity by an
historically isolation due to a marine barrier during the formation of
the Isthmus of Tehuantepec in the late Pleistocene (Vázquez-Miranda et
al., 2009). The correlation between genetic and acoustic distances, and
the pattern of isolation by distance previously reported in the
white-eared ground-sparrow (Rodríguez-Bardía et al., 2022), suggest an
important role of cultural drift or sexual selection (Camacho-Alpízar et
al., 2018; Irwin et al., 2008; West-Eberhard, 1983). White-eared
ground-sparrow uses solo songs for female attraction, and males, after
learning songs are not able to learn new songs (Sandoval et al., 2016;
Bonilla-Badilla 2021). Thus, if females are choosing specific acoustic
traits, specific song types or young males are imitating specific songs
in each population, a specific phenotype would be favored over
generations (West-Eberhard, 1983). For example, female great tits,Parus major, prefer males that emit song types with higher
frequencies in noisy environments (Halfwerk et al., 2011). In this
context the higher frequencies in urbanized populations and the
different dialects among populations of white-eared ground-sparrows
(Méndez et al., 2020; Sandoval et al., 2016; Sandoval & Mennill, 2014;
Bonilla-Badilla 2021), could be reflecting sexual selection acting over
populations.
Morphology
The female body size of white-eared ground-sparrow decreases in MTV and
JBL as well as males of JBL population along the sampling periods. Body
size often decreases in response to a decrease in food availability and
quality (Goodman et al., 2012; Salewski et al., 2014; Yom-Tov & Geffen,
2011). Introduced species such as rats and mice may compete for food
resources of our study species. A similar reduction in body size was
observed in the lesser sheathbills Chionis minor, in Marion
Island, due to the introduction of rats and cats that eat terrestrial
macro-invertebrates, the sheathbills primary food resource (Huyser et
al., 2000). In white-eared ground-sparrows reduction in body size may
also be caused by lower-quality food as a result of urbanization
(Mennechez & Clergeau, 2006). Higher predation risks could also play an
important role in size reduction, because smaller individuals may be
better able to avoid cats and other predators (Seress et al., 2011).
Given that sparrows are a common prey of cats (Seress et al., 2011;
Yom-Tov & Geffen, 2011), this would be an important adaptation (or
selection process) for ground-sparrows facing urbanization.
In JBL males increased the exposed culmen length and decreased beak
width between sampling periods. Due to the widespread use of bird
feeders, the trend toward longer beaks has been linked to the
consumption of larger prey or generalized feeding (Bosse et al., 2017;
Hüppi & Geiger, 2022; Rolshausen et al., 2009). In great tits,Parus major, an increase in birds with longer beaks was
associated with an increase in fitness, because birds were able to feed
from bird feeders (Bosse et al., 2017). A decrease in beak width
reflects a decrease in bite force (Badyaev et al., 2008). For example,
the house finches Haemorhous mexicanus that inhabit urban
populations in Arizona have a narrower beak, and less bite force,
because they consume softer human food.(Badyaev et al., 2008; de León et
al., 2011; Hüppi & Geiger, 2022). In contrast, in MTV males decrease
their exposed culmen length and increase their beak width. The increase
in beak width reflect that birds are likely consuming larger and tougher
food, which would require an increase in bite force (de León et al.,
2011; Hüppi & Geiger, 2022). Differences in beak lengths between
populations may also be the result of individuals consuming novel foods,
regardless of the morphology of the species; indicating adaptation
toward exploiting different food resources (de León et al., 2011; P. R.
Grant & Grant, 2002).
Comparing four populations of white-eared ground-sparrows over a decade
revealed changes in levels of inbreeding, spectrotemporal song
characteristics, and morphological traits. Interestingly, we only found
a positive relationship between differences in genetic divergence among
populations and song divergence. We suggest that this correlation
corroborates the role of urbanization as a barrier for white-eared
ground-sparrows. The correlation may also be explained by cultural drift
or sexual selection, as it is possible to observe changes in acoustic
signals associated with genetic divergence if selection for song
preferences acts continuously in populations (Irwin et al., 2008;
Sathyan et al., 2017). The relationship between genetic and phenotypic
traits is often slow and complex, due to the different forces acting at
the same time (Irwin et al., 2008; Carnicer et al., 2009; Sathyan et
al., 2017). Only long-term studies in urban environments shed light on
the processes of adaptation of different species to the drastic changes
imposed by urbanization, since species with different life history
traits may response and adapt in different ways to the same
environmental changes (Rodríguez-Bardía et al., 2022).
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Table 1. Results of principal components analysis of solo songs of the
white-eared ground-sparrow Melozone leucotis . The asterisk
indicates the variables that have a larger contribution in each
component.