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.