Introduction
There are a number of review articles published which discuss the adaptations of animal species to urban habitats with a general census that microevolutionary adaptations are possible in urban populations given the novelty of selection pressures which urban habitats provide and despite the relatively short time period in which urban populations would have colonized them (Erz, 2010; Lowry et al., 2013; Mcdonnell & Hahs, 2015). Phenotypic plasticity, the ability of organisms to change phenotypic traits in response to their environment in their lifetime (Stearns, 1989) is a mechanism which is expected for individuals to demonstrate upon colonization of new habitats. It has been noted that terminology surrounding these concepts should be carefully considered when discussing adaptation to urban environments. For example, Mcdonnell and Hahs, (2015) define the terms adaptedness and adaptation, explaining that phenotypic plasticity can allow certain animals to be pre-adapted to tolerate new environmental conditions and that the phenotype presented in this case can remain temporary or result in changes in genotypes (microevolutionary adaptation). Likewise, Lowry et al. (2013) agree that genetic changes are essential to accompany parallel observed phenotypic changes in order to gage if adaptation has occurred. It is also important to remember that if these changes (genetic or otherwise) do not result in a fitness advantage for those living in urban habitats, then they may not be considered as adaptations (McDonnell & Hahs, 2015).
Birds have been the most extensively studied animals in urban habitats, particularly in areas of Europe and North America (Erz, 2010). Urban birds have shown many behavioural changes in urban habitats, but many can only attribute to phenotypic plasticity. While species such as the European blackbird (Turdus merula) and has retained significant focus by researchers and has shown indications of physiological adaptation with a genetic basis (Mueller et al., 2013), the white footed mouse (Peromyscus leucopus) also presents a promising case (Harris & Munshi-South, 2016).
Bird vocalization
Studies have found bird species which have shown divergence in their vocalizations across urban and rural populations. These include white crowned sparrows (Zonotrichia leucophrys) (Luther & Baptista, 2010), silvereyes (Zosterops lateralis) (Potvin et al., 2014) and the European blackbird (Turdus merula) (Mendes et al., 2011). One interpretation of this divergence is that urban populations have adapted to the increased anthropogenic noise in urban areas where singing at a higher pitched frequency mitigates low frequency traffic noise (Nemeth & Brumm, 2009). Observations of such vocalization’s patterns along a gradient of urbanization and anthropogenic noise in European blackbirds would support this (Mendes et al., 2011), however other species, such as the silvereye, actually show the opposite trend where vocalizations of urban individuals are at lower frequencies than that of their rural conspecifics (Potvin et al., 2014). There has been debate over the mechanisms behind these observations and while there is argument for cultural evolution (change in a learned behaviour trait from one generation to the next) (Luther & Baptsita, 2010) and phenotypic plasticity (Mendes et al., 2011) there is no evidence to suggest that the divergence has a genetic basis. In fact, genetic analysis has shown that the urban and rural populations of Silvereyes (Potvin et al., 2013) and European Blackbirds (Partecke et al., 2006a) show no genetic differentiation. In a review by Lowry et al. (2012), the importance of addressing the extent in which genetic adaptation in urban animal populations has occurred was highlighted. Furthermore, there are no studies which demonstrate that the divergence of vocalization in urban individuals results in a fitness advantage in urban habitats, another key piece of evidence for adaptation highlighted by Mcdonnell and Hahs (2015). The literature would currently suggest that the divergence in bird song is associated more so with behavioural plasticity than any type of evolutionary adaptation.
Bird Physiology
A more convincing case can be summarised for literature regarding possible adaptations in bird stress physiology, though gaps are also present. For both the European blackbirds and dark-eyed junco’s (Junco hyemalis), levels of the stress hormone, corticosterone (CORT), have been found at significantly lower levels in urban compared to rural populations (Partecke et al., 2006b; Atwell et al., 2012) and this is thought to be an adaptive response to cope with heightened exposure to stressors in urban habitats (Partecke et al, 2006b). Contradictorily, a similar study with house sparrows (Passer domesticus) concluded that CORT levels were higher in urban individuals than rural ones (Beaugeard et al., 2018). Differences here are likely to be due differences in the methods for obtaining CORT levels. For both the blackbird and dark-eyed junco the degree of urbanization was tested against CORT levels in the blood plasma while that of the house sparrow was limited to CORT levels in the feathers (which do not correlate to that in the blood plasma) (Beaugeard et al., 2018). With this in mind, the house sparrow experiment may not provide significant evidence with regard to adaptation. In all three bird species, the limitations are derived from using juveniles. For the house sparrow, CORT levels in blood plasma varies during development and nests are hard to access in cities so CORT levels in feathers were used instead (Beaugeard et al., 2018). Meanwhile, the blackbird and dark-eyed junco experiments are also limited in their own ways, particularly in regard to supporting the argument for a genetic basis in the observed differences in CORT levels, as “early developmental effects could not be ruled out” since subjects spent part of their early life in natural habitats (urban or rural). In spite of this, a candidate gene study by Mueller et al. (2013) found that a gene associated with anxiety, harm avoidance, novelty seeking and stress sensitivity in blackbirds was significantly associated with habitat type (rural or urban). It has also been found that a population of dark-eyed juncos colonising an urban habitat were significantly different from populations in natural habitats both morphologically and genetically, though specific differences in candidate genes i.e. for stress, were not tested (Rasner et al., 2004). For both the dark-eyed junco and house sparrow, it is suggested that candidate gene studies which identify genes associated with stress and test for differences here between rural and urban populations should be conducted in order to gage if these differences are phenotypic plastic or have resulted in heritable genetic changes.
Mice Physiology
Such candidate gene studies as well as genome wide studies have been conducted in white footed mice in New York City by Jason Munshi-South and Stephen Harris. Their studies have identified signatures of positive selection in candidate genes associated with metabolism where genetic differentiation had occurred between urban and rural populations (Munshi-South & Kharchenko, 2010; Harris & Munshi-South, 2016) suggesting that urban populations might have adapted to novel diets. Morphological differences have also been found in the skulls of urban and rural white footed mice where urban individuals were found to have shorter upper and lower tooth rows than rural ones and this is likely associated with diet as well (Yu et al., 2017). These findings would suggest that the urban white footed mice are adapting to novel diets in their new environments, specifically, the differences in skull morphology suggest that urban mice are consuming food that requires less chewing than that of their rural conspecifics while the genetic analysis reveals that urban diets may include higher fat and carbohydrate content (Harris & Munshi-South, 2017). While these changes have occurred, there are no studies which examine the relative diets of urban and rural white footed-mice and which determine if differences in diets, and consequently genetic changes in metabolism, actually result in a fitness advantage for urban mice exploiting the novel habitat. Furthermore, another genetic study found that the urbanization of white-footed mice is negatively associated with genome-wide variation, reducing the evolutionary potential of urban populations (Munshi-South et al., 2016). This leads to an important conservation question that even if the white-footed mouse populations are adapting to urban habitats i.e. through diet, are these adaptations enough for their populations to be stable and thrive? Overall, despite there being evidence of both phenotypic and genetic change in the urban populations of the white footed mouse, it is questionable as to whether they are actually adapting and if so, is it in enough time to avoid to local extinction (McDonnell & Hahs, 2015).
Conclusion
Both the blackbird and white footed mouse show promise for future research in understanding adaptation to urban habitats as they exhibit phenotypic divergence in morphology and physiology and have also shown changes at the genetic level which are specific to these divergences. Despite this, there is a lack of holistic consistency in the literature which draws phenotypic and genetic divergence together with an established fitness advantage in order to appropriately determine adaptation to urban habitats. While there is also question over these possible adaptations enabling populations to thrive in urban habitats, continued monitoring of the already detected divergence of these species between their urban and rural populations as well as factors of conservation concern i.e. overall genetic variation, should continue to be monitored so as to ensure that populations are not at an unnoticed risk of local extinction in urban habitats.
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