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Abstract

As cities around the world grow, urbanization increasingly threatens ecosystems. Urbanization contributes to habitat change, pollution, the loss of biodiversity and makes ecosystems more vulnerable to environmental change. Birds are an example of organisms that are experiencing the effects of urbanization. One way they are being affected due to environmental change is through a shift in their coloration. Their colorful plumage is due to consuming carotenoids, which also aid in survival mechanisms. However, the carotenoid sources are decreasing as urbanization continues. Therefore, the rural birds are brighter and urban birds are becoming duller. A major example of a bird species being affected by urbanization is the great tit (Parus major). A decrease in pigmentation leads to less picky female birds, as they cannot discern which male bird is most fit. As a result, populations will decrease forming an inbreeding depression and their immune systems will be dampened. The great tit population is also likely to speciate under these new urban conditions. The model for the dynamic is that urbanization brings effects that lessen bird pigmentation, then urban birds continue to mate which brings forth more and more dull birds, thus radiating the genes for less bright plumage, and lowering bird populations. The aforementioned model can be applied to the blue jay (Cyanocitta cristata).

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Humans play a large role in eco-evolutionary feedbacks by furthering urbanization (Alberti 2015). Urbanization comes in many forms and includes many downstream effects on wildlife. The process of global urbanization is where human populations’ consumption, material demands of production, and urban waste discharge become more severe with time (Cai et al., 2017). Urbanization moves quickly– it was projected in 2007 that two-thirds of the human population are expected to live in cities within the next thirty years (Bradley and Altizer 2007). The effects of urbanization in the context of wildlife are an alteration of resource availability, community composition and land use (Murray et al., 2019). The species affected need to quickly learn how to both live with and fight against human caused changes, or their populations will suffer (Salmon et al., 2016). 

Anthropogenic disturbances on carotenoid availability can affect a bird’s choice of mate by changing the visual cue which aids in the decision (Eeva et al., 2002).  Less pigment limits how desirable the birds are, because coloration is sexually selected for (Saks et al., 2003). Pollutants can alter sexually selected bird coloration (Grunst et al., 2020). The expression of secondary sexual characteristics is very sensitive to stress because they are subject to phenotypic plasticity (Dauwe and Eens., 2008). Metals are an example of a pollutant that can often be released into the environment through anthropogenic activities (Giraudeau et al., 2015). That said, one example of a downstream effect is how pollutants have the power to indirectly affect birds by changing their plumage color (Eeya et al., 2002). As a concrete example, a recent study by Pacyna et al. (2018) noted that the phenotypic expression of bird’s pigmentation can be altered by metal contamination that stems from pollution.

Carotenoids are responsible for the vast majority of the coloration within bird plumage (Pacyna et al., 2018). The carotenoids enter the organism’s body by being directly ingested, and they are the most frequent pigments that are used in animal signaling (Hill et al., 2002; Svensson and Wong 2011). For example, the red, orange, and yellow pigments often seen on birds are due to carotenoid presence (Saks et al., 2003). In their environment, the birds will sequester the colors in specific patches on their feathers to advertise themselves sexually, or to engage in competition with other birds (Saks et al., 2003). For example, in male house finches, carotenoid consumption is what determines how bright the birds’ feathers are (Hill et al., 2002). Male finches use their brighter coloration to their competitive advantage. Thus, when their pigmentation is not as strong their ability to compete decreases and thus so does their fitness. 

Bird coloration is subject to change alongside the increase in urbanization (Sillanpaa et al., 2008). Studies have demonstrated that carotenoid-based coloration in wild birds is negatively associated with increased exposure to such pollution (Giraudeau 2015). It has been shown that there are lower amounts of carotenoids in urban areas when compared to rural areas (Isaksson 2009).  A study by Jones and their colleagues (2010) noted that the brightness of the plumage in male birds declined in relation to how much urban life was surrounding the forests where the cardinals breed. This pattern is due to how pollutants in the environment can limit the amount of food items that harbor the most carotenoid molecules (Eeva et al., 2002). Evidence for this is seen when looking at rural and urban nestlings; the plumage of the rural nestlings was a vibrant yellow compared to the urban ones (Biard et al., 2017). 

A popular bird used to study the effects of urbanization on plumage pigmentation is the great tit (Parus major). The male great tit is identifiable by its large and central black breast stripe (Norris, 1990). Another key visual feature of the male great tit is bright yellow patches on their chest. Green can also be found around their upper wing area. A study by Giraudeau and their colleagues (2015) measured the concentration levels of eight pollution metals in the plumage of the great tit. The researchers also then assessed to what extent the metals were tied to carotenoid pigmentation (Giraudeau et al., 2015). The results indicated that carotenoid pigmentation in the great tit was negatively associated with the amount of mercury present, i.e., pollution. 

There are costs and benefits to the mate-choice system in birds based on the coloration of their plumage. In the great tit bird population, bright male plumage is an indicator for good health and fitness, which the female recognizes. Thus, in their typical natural environment, the duller males, indicating less fitness, do not get mated with, and their bloodline dies off allowing for only the fittest to proceed in forming their population. Benefits of putting energy into sexually selected traits are increased mating success and quality (Candolin 2019). However, in a mate-choice system such as this one, there must be a balance between energy division. Brighter plumage isn’t always better. Some costs are that fitness mechanisms use up resources and energy at the expense of other key traits like growth and the possibility of an early death (Candolin 2019). 

In birds, coloration can be a good adaptive feature, but only to a certain point. Coloration can be used to evade predation, engage in intraspecific or interspecific communication, resist bacterial damage, and thermoregulation (Toral et al., 2008). Coloration’s role in sexual selection is connected to the tradeoff between the divvying of carotenoid molecules to color signals, and then to other survival processes (Saks et al., 2003). For example, Sumasgutner and their colleagues (2018) measured how coloration due to carotenoid content varied in urban communities. The researchers explain how the inner-city dwelling kestrels are more affected by urbanization than the outer-city birds. The inner-city birds allotted more of their carotenoid store for health use, not pigmentation (Sumasgutner et al., 2018). Thus, the birds with less pigmentation put more energy into overall survival, as their carotenoids were siphoned into survival mechanisms. However, their likelihood of mating would be expected to decrease, and so would their fitness.

When sexually selected for traits become null, the method for indicating the fitness of a mate becomes obsolete, and consequently unfit offspring arise. There is a pattern that demonstrates when cues disappear, less-careful mate choices arise with the female birds (Candolin 2019). When all the great tit males in the vicinity become dull, the females have no choice but to randomly mate because their cue for who they should pick has disappeared. Thus, the risk of mating with an unfit male increase. Unfit males will yield fewer fit offspring due to the passing on of their unfit genes. Unfit offspring will likely not survive and so the female suffers fitness reductions, such as an unnecessary energy expenditure, in light of the mate-choice system changing (Candolin 2019).

A decrease in sexually selected for characteristics can greatly affect overall population size resulting in the Allee effect. If and when the unfit individuals born do survive, they will continue to produce unfit offspring (Candolin 2019). As the trend continues, the species will continue to become less and less fit, and eventually more and more will die off. Even if some of the offspring are viable enough to survive into adulthood, the population can still decline (Candolin 2019). The Allee effect, when there is a lower male encounter rate in smaller populations, can occur in this situation (Candolin 2019). This effect will only continue to whittle away the population numbers as eventually, males will be harder to find for the females and they cannot reproduce. 

When a population decreases severely enough in a region, there is likely to be inbreeding. An inbreeding depression will often lead to a decrease in overall population fitness (Szulkin et al., 2009). The traits that are most likely to decline with an inbreeding depression are ones that relate closely to the fitness of the organism (Crnokrak and Roff 1999). For instance, reproductive traits like the number of eggs that are laid, or the number of offspring that survive are likely to be altered (Crnokrak and Roff 1999). When a population declines significantly, mate options become sparse. An already decreasing population will only find themselves in a deeper hole if less fit members, who are also genetically related, breed. A study was done on the great tit by Szulkin and their colleagues (2009) to see if the birds from a given population will resist mating with their related kin. To do this, they created four models based on the great tits which compared random mate choices with varying levels of mate availability by year (Szulkin et al., 2009). The models projected over forty years of inbreeding coefficients (Szulkin et al., 2009). As a result, they found that the great tit will not avoid mating with kin (Szulkin et al., 2009). Thus, an inbreeding depression is likely to occur in the urban great tit species.

Research has found that the molecules that make up carotenoids have vast fitness functions, as well as phenotypic and physiological functions (Girardeau et al., 2015; Svensson and Wong 2011). Carotenoids have the ability to protect the vital nervous system from oxidative damage and can also stimulate the organism’s immune defense (Saks et al., 2003). As mentioned in Sumasgutner et al. (2018), the harsh city environment requires more of the carotenoids to be used for immune and physiological responses in lieu of pigment. Therefore, in response to urbanization the birds are allocating less of their carotenoids to coloration and more to overcoming the challenges in the new urban environment. 

Immune response and great tit plumage coloration are positively related, which poses a threat to the health of dull great tits. A study by Dufva and Allander (1995) tested if the intensity of the great tit’s yellow coloration reflects their leukocyte count, which is a measure of immune response. They found a positively related correlation between the overall amount of heterophils, a type of leukocyte, and color intensity (Dufva and Allander 1995). In this study, the elevated heterophil counts in bright males indicates an absence of blood parasitism (Dufva and Allander 1995). Thus, a high heterophil count means that they have high immunocompetence to fight infection (Dufva and Allander 1995). Based on this study, there is evidence that dull male birds will be less fit, and thus as a unit the population will suffer further due to immune incompetence. A similar finding also states that the kestrels with less coloration, thus less carotenoid pigment, had a higher intensity of parasitism (Sumasgutner et al., 2018). 

Oxidative stress from air pollution can hinder the sperm quality of male great tits, and thus their population size is affected. Oxidative stress is defined as “the imbalance between oxidants and antioxidants in favor of the oxidants, potentially leading to damage” (Sies, 2000).  Indirect effects of pollutant metals in the atmosphere cause oxidative stress to great tits by increasing the creation of reactive oxidation species (Koivula et al., 2011). As it turns out, the sperm of more colorful male birds are better protected against oxidative stress from extrinsic factors like pollution (Helfenstein et al., 2010). In a study done by Helfenstein et al. (2010), it was found that duller males had a larger reduction in the motility and swimming ability of their sperm. Weak sperm decreases the likelihood of successful conception with a female mate. When carotenoid supplementation was given to the dull birds, they showed an increase in sperm quality (Helfenstein et al., 2010). Thus, more colorful great tit males will have more efficient and healthy sperm compared to their dull counterparts. Therefore, if the great tit is suffering from a decrease in carotenoid consumption due to urbanization, then they will also produce less viable offspring and the population will decline further.

Phenotypic plasticity is a mechanism of genetic evolution. Price et al. (2003) ran a study on birds that looked at the evolution of red and yellow carotenoid coloration, and then the evolution of their foraging behaviors on islands. Moderate levels of plasticity are functional in furthering population survival in a new environment and have the ability to speed up evolutionary change (Price et al., 2003). The moderate levels of plasticity succeed in becoming permanent when many traits, a mix of plastic and non-plastic, create a trait that is included in an adaptive response (Price et al., 2003). The researchers concluded that moderate levels of phenotypic plasticity in terms of coloration have the ability to bring forth genetic evolution in bird plumage coloration (Price et al., 2003). 

Bird coloration is a genetic trait, thus it is subject to evolution. A study by Gazda et al (2020) looked to understand the genetic mechanism that determines sexual dichromatism in birds. Sexual dichromatism is when male and females have different pigmentations because of sexual selection. The goal of the research was to determine if carotenoid-based dichromatism in canaries is controlled by a gene that is responsible for encoding the enzyme that cleaves carotenoids (Gazda et al., 2020). Using transcriptome analyses, Gazda et al. (2020) concluded that the difference in the sex’s pigmentation is due to how the carotenoids are degraded. The suggestion based off the result is that the colorations between sexes have the ability to evolve through molecular mechanisms by genes (Gazda et al., 2020). Thus, the shift in the phenotype for birds in urban environments could stabilize as an evolved trait. 

Urbanization drives speciation (Halfwerk 2020). The process of urbanization is very disruptive to the natural world. Changing the landscape has the ability to change sexual selection pressures (Halfwerk 2020). This, of course, would include the great tit females’ mating based on male plumage pigmentation. Altering sexual selection is theoretically necessary precursor for sympatric speciation (Halfwerk 2020). Therefore, the emerging dull great tit phenotype could signify the start of a speciation event. That said, the increase in pollution leading to decreased plumage pigmentation can lead to a divergence in the populations (Candolin 2019). In ecological systems, speciation occurs when there is natural or sexual selection pressures between two different environments (Halfwerk 2020). Populations exposed to extrinsic changes have been found to emphasize different cues (Candolin 2019). For the great tit, there may be areas where some live where pollution is not intense enough to alter their carotenoid levels, and some areas where it is. The anthropogenic disturbance thus guides the potential speciation through a differentiation in mate-choice cues, and thus a split in their mate choices (Candolin 2019). Thus, should pollution continue to affect the great tit’s coloration, their species could evolve to differ enough to speciate. 

Scientists can use a model to explain the effects of the eco-evolutionary dynamic in other species. A model of this dynamic includes how urbanization brings forth pollution and less carotenoid sources, so that the birds can’t synthesize as much pigmentation, and then they become duller and less fit in terms of selection. The theme that carotenoid pigmentation decreases in relation to heightened levels of urbanization is relatively consistent between the great tit, finch, and cardinal. Three bird species displaying the same pattern is no longer a coincidence. Thus, perhaps the model can be applied to another bird, like the blue jay (Cyanocitta cristata). Blue jays are known for their bright blue plumage. The bird mainly resides in eastern North America, which has a high concentration of cities. If the model is correct, then it seems as though researchers should expect for the blue plumage of the blue jay to become duller as a result. It can also be predicted that their populations will crease. 

In conclusion, urbanization’s effect on carotenoid availability is altering the pigmentation of the great tit. Since the pigmentation of male great tits is a sexually selected trait, there are multiple downstream effects of dullness. One example is that the female birds will be less picky with their mates due to how their usual selection process based on plumage has been erased. With random mating comes a less fit population. Populations that become less fit are more prone to decline, inbreeding, and disease due to a decreased immune system. Another downstream effect is that the change in pigmentation will lead to a population divergence among great tit populations. Using modeling, the effects of urbanization on plumage coloration can be applied to many other species, like the blue jay. 

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