Avian Egg Coloration and Visual Ecology

Evolutionary processes have generated diverse color patterns of avian feathers, skin patches, and egg shells, which perform countless functions, including mimicry, crypsis, prey detection, predator avoidance, and signaling individual identity or mate quality (Hill & McGraw 2006). If color patterns function to communicate information, then do we need to understand the sensory and perceptual systems responsible for detecting these complex patterns? Recent technological and theoretical efforts have revolutionized the study of avian vision so that we now can use genetic sequencing of the opsin genes involved in avian color vision to reconstruct light-receptor sensitivity parameters, and this information can be used in perceptual models of birds' vision. Combined, these two approaches allow for a better understanding of the role that visual ecology plays in the evolution of avian communication and recognition systems, especially in the study of egg mimicry, ultraviolet (UV) light sensitivity, and their role in shaping the sensory ecology and behavioral patterns of diverse bird species (Hubbard et al. 2010).

Why do bird eggs range in color from uniformly white to brightly colored and/or densely speckled (maculated; see Banner photo)? Based on a comparison of eggshell patterns between different avian families, one of the most prevalent ecological factors responsible for the diversity of egg coloration is the interaction between brood parasites and their hosts (Kilner 2006). Obligate brood parasitic birds lay their eggs in nests of other species, thereby imposing a cost on hosts to raise genetically unrelated young (Davies 2000). Egg coloration and maculation play important roles in whether hosts accept or reject the fitness costs imposed by parasitism. For example, the blackcap (Sylvia atricapilla) is a host of the parasitic common cuckoo (Cuculus canorus) in Europe and typically rejects all non-mimetic (dissimilar) eggs (Honza et al. 2004). By experimentally parasitizing blackcap nests with host-like mimetic eggs (using eggs of other blackcaps), egg rejection drops to 36% (Polacikova et al. 2007). Accurate rejection of foreign eggs even at seemingly low rates can still be an adaptive behavior because the host reduces its chances of spending time and energy raising overly needy and genetically unrelated offspring.

These and other cuckoo hosts appear to have evolved a simple rule of thumb to direct their behavior: "eject the egg unlike your own". But how does a bird know what its own eggs look like? Researchers have tackled this question by experimentally manipulating the appearance of the bird's own egg by dying one, more, or all eggs in the same brood (Figure 1). Such studies reveal that great reed warbler (A. arundinaceus) hosts rely on both color differences between eggs and learned memories of their own eggs to recognize and reject cuckoo eggs (Moskát et al. 2010).

Truly astounding, though, is that selection for visual cues of recognition has resulted in the evolution of extreme level of egg color mimicry of specific hosts by different parasitic cuckoos (Figure 2). Through the process of coevolutionary arms race, egg mimicry also has likely influenced the perceptual sensitivities of hosts and their abilities to correctly identify and reject foreign eggs from the nest. The perceptual acuity necessary to make a correct rejection invites direct investigation; researchers can experimentally parasitize the nests of hosts with eggs of varying degrees of similarity, in order to determine the thresholds in color and maculation at which hosts make decisions to reject dissimilar, and likely foreign, eggs from their nest.

Before an experimenter can set out to manipulate egg colors, especially the ones hypothesized to be important for foreign egg rejection, it must be first established which colors that host species can see. The cone photoreceptors of the vertebrate retina (Figure 3) are responsible for color vision. The genes for opsins encode specific photopigments expressed in these cones, generating different combinations of proteins with maximal sensitivities to a particular wavelength of light (λ_max). The cone cells of all color-sensitive vertebrates express opsins. The number of different opsins that an individual possesses is related to the number of colors to which it is sensitive.

Avian retinas differ from those of mammals in many ways, notably in the number of cone types that they possess. Unlike mammals, which typically have only two or three different cone types (Figure 4), bird species possess 4 distinct single cone types in their retinas, making them tetrachromatic (Figure 5; Hunt et al. 2009). Tetrachromats are theoretically able to see twice as many colors as trichromats (e.g., humans). For example, two eggs might appear indistinguishable to us, but a bird might see them displaying two distinct colors. This has direct implications for scientific investigations of avian perception — how can we manipulate egg colors when birds themselves may be more sensitive than we are to subtle differences in color?

Some avian lineages, including many passerines, are able to see light in the ultraviolet (UV) range, which humans cannot see (Hart 2001). The hosts of brood-parasitic cuckoos in Europe and brown-headed cowbirds (Molothrus ater) in North America are passerines, implying that they might be able to perceive cryptic (to human) UV differences between their own and parasitic eggs to discriminate and reject parasitic eggs. One of the types of opsins (SWS1) is sensitive to the shortest wavelengths of light, and is found in all vertebrate classes (Hazel et al. 2006). In humans and many bird species, the SWS1 opsin is expressed in cones that respond maximally to violet light (such species are termed violet-sensitive, VS). In some passerine species, however, the SWS1 opsin gene codes for a photoreceptor with a λ_max that crosses into the UV portion of the light spectrum (Figure 6). Species with this type of SWS1 cone are UV-sensitive (UVS; Hart 2001; Ödeen & Håstad 2003; Hunt et al. 2009).

A UV-sensitive SWS1 is apparently ancestral among vertebrates, but was subsequently lost in primates and birds (Yokoyama 2000; Jacobs & Rowe 2004; this is a great review for those interested in the evolution of color vision in vertebrates). Among birds, however, UVS has re-evolved independently at least 4 times via a shift in SWS1 sensitivity (Hunt et al. 2009). UV-sensitivity in turn can serve a number of adaptive behavioral and ecological functions, including sexual displays, predator/prey detection, intraspecific communication to avoid detection by VS predators (Håstad et al. 2005), and defense mechanisms against egg mimicry in brood parasitism (Honza et al. 2007; Underwood & Sealy 2008). These two latter studies demonstrate that the UV-reflectance of eggs differs between host and parasite, suggesting that hosts can use UV-only visible patterns to discriminate between their own and foreign eggs. Whether UV-sensitivity evolved as a response to brood parasitism or was already available for hosts to utilize at the onset of their evolutionary history with brood parasitism, remains still unknown (Underwood & Sealy 2008).

Regarding other ecological contexts, eggs of cavity-nesting species tend to have higher UV-reflectance than eggs of open cup nesters (Aviles et al. 2006), providing further evidence that UV light can both be seen and be informative for parental birds' behavioral decisions. Accordingly, cavity-nesting spotless starlings (Sturnus unicolor) are more likely to accept experimental eggs placed just outside the nest cup within the cavity (by pulling them them into the nest) with high UV-reflectance than eggs with low UV-reflectance.

But how can we know whether the SWS1 opsin of a particular bird species will be maximally sensitive to UV or violet wavelengths of light? Much of our knowledge of the avian sensory world now derives from physiological and molecular techniques which describe the sensitivities of opsins present in the eye. The traditional method of microspectrophotometry allowed researchers to determine the λ_max of any photoreceptor by transmitting light through it and measuring which wavelengths are absorbed (Govardovskii et al. 2000). More recently, DNA sequencing of the SWS1 opsin gene has allowed researchers to assign VS/UVS states in a more cost-effective and non-lethal manner, relevant for large scale comparative studies (Ödeen & Håstad 2003), including work with bird species of conservation concern for which invasive studies cannot be done (Igic et al. 2010).

The molecular machinery of the SWS1 photoreceptor requires only one amino acid substitution in a select few sites of the protein's amino-acid chain to change a VS species or individual to a UVS species or individual (Yokoyama et al. 2000). Genetic sequencing of the SWS1 opsin gene is now regarded as an accurate, reliable and economical alternative to microspectrophotometry (but see Smith et al. 2002).

Integrative research spanning the fields of molecular genetics, physical light reflectance measurements, and behavioral experiments, has allowed researchers to quantify color patterns as birds would see and use them (Vorobyev & Osorio 1998; Endler & Mielke 2005). To interpret physiological and genetic data, however, requires perceptual models which are mathematical representations of what a bird can see, based on a number of different parameters, including the amount of light that reaches the retina and the relative abundance and type of photoreceptors present in that particular species' eyes. Using physiological data generated from genetic sequencing of the opsin genes (Ödeen & Håstad 2003), researchers can now produce reasonably accurate models of avian visual perception and its behavioral implications in egg rejection decisions (Cassey et al. 2008). Typically, the light reflectance of surfaces of interest, such as eggshells, is measured with a spectrophotometer and the resulting relative light reflectance data are then filtered through the perceptual model's equations to assess whether a species in question can see differences between particular light reflectance patterns, or colors.

Perceptual modeling has been adapted to study a wide range of phenomena; these include the perceived variability in eggshell colorations across many bird species (e.g. Cassey et al. 2009; Cassey et al. 2010), the adaptive use of human-made refuse as nesting material (Igic et al. 2009), as well as sexual dimorphism (Igic et al. 2010). Future studies of perceptual modeling should focus on the differences in egg colors between brood parasites and their hosts, and whether or not hosts are visually equipped to perceive these differences. Overall, molecular techniques and sensory modeling now allow researchers to begin to study the mechanisms underlying avian color vision, and do not require severely invasive methods. These integrative approaches make it possible for future researchers to accurately describe and manipulate salient color information in studies of mimicry, crypsis, mate quality, and other behavioral functions critical for survival and reproduction across diverse species of birds and other visually oriented animal lineages.