Evolution of sexual selection in birds
Sexual selection is the component of natural selection that involves the evolution of characteristics with no inherent advantage to the individual itself, but which are involved in the success of passing on genetic information during reproduction. In this way sexual selection directly affects an individual's fitness i.e. the ability of an individual to produce offspring with the same genotype and hence the same phenotypic features of the individual in question. These features may be apparently useless when first looked at but they increase the bearer's chances of either attracting a mate or competing with other individuals for one, therefore increasing chances of reproductive success. The improved ability to attract mates is called intersexual selection while the improved capability to compete for mates is called intrasexual selection (Sadava et al., 2008). It is thought that females may select a male due to his high-quality phenotype in order to pass along part of his genome to her offspring, who will then be preferred by other females, her assessment requires sexually selective cues which I will discuss.
Sexual characteristics such as bright colours, long tails and overly elaborate courtship displays are typically found in the males of many species, with the females as the 'choosing' sex. These characteristics can even be detrimental to the individual itself, but these act to show potential mates that the individual has the resources and the strength to support this disadvantageous quality (Jennions et al., 2001). One example of this was shown by Andersson & Andersson (1994), in African long-tailed widowbirds (Euplectes progne) in which the length of the tail of the bird is a sexually selected trait, individuals with longer tails (within normal limits) are more successful at attracting females and fathering nests than individuals with shorter tails. The longer tailed individuals actually have to develop a larger wingspan in order to compensate for the detrimental effects to flying of the long tail so this sexual characteristic is not without its costs.
Another example of this cost of expressing traits of sexual selection is demonstrated by Parejo & Aviles (2007); they found that avian brood parasites may actually pick up on these sexual signals to determine the quality of potential 'foster' parents for their own offspring. They eavesdrop on the conspicuous signals present as sexual ornamentation or other sexually selected traits to assess the parental quality of conspecifics within a given host species. In this way, there is another cost to bear for increased sexual selection.
Conspicuous behaviour from males attempting to attract female mates can sometimes put them at a higher risk of predation, this can be seen in a study by Mougeot & Bretagnolle (2000) in which they looked at predation of petrels (particularly the blue petrel - Halobaena caerulea) by a major avian predator - the skua (Catharacta antarctica lonnbergi). Petrels use calling to attract mates, which poses a danger as it exposes them to the skuas looking for a meal. Using playback devices they were able to show that skua used these calls to locate petrels. It was also found that the petrels used the calls of skuas in order to deduce the risk of predation and hence to stop their calling, and reduce their own conspicuousness.
Sexually selected traits can give females an insight to the health of a potential male mate. For example, Birkhead et al. (2003) used the fact that female zebra finches prefer males with brighter coloured bills to test if this was also a way in which they indirectly assessed a male's immunocompetency. The colour in the bill is a result of carotenoid pigments, these are absorbed from the finch's food (they cannot be synthesised by the finch). Carotenoids are also components of the immune system, it can be said that males in good health require fewer carotenoids for their immune system than those in poor health, in this way they are able to 'afford' to use more of the carotenoid pigments in the colouration of their bill. This was proved when the researchers injected phytohemagglutinin into the birds' wings, this produces a reaction from T-lymphocytes and ultimately a thickening of the skin in the area injected. Males with higher levels of carotenoids (and hence, brighter coloured bills) developed thicker skin than those with lower levels - showing a healthier immune system. Females who choose the males with brighter coloured bills know that they are less susceptible to disease and parasites, and better equipped to raise offspring.
Another example of sexually selected features giving an indication of relative health can be seen in the ability of avian partners to build a nest. Soler et al. (1998) tested this theory and found that species in which both sexes work to build a nest (simultaneously assessing the other's quality) will build larger nests as each partner wishes to demonstrate their qualities, it was also found that those species in which both sexes work together to build a nest invest more in reproduction; hence it was found that species with larger nests relative to their body size invest more energy and time in reproduction and parental duties. It can be said that nest-building is a component of sexual selection. Palomino et al. (1998) somewhat supports this conclusion but they found that in Rufous Bush Robins (Cercotrichas galactotes) the nest-building exercise is a "post-mating sexual display" that demonstrates the readiness of the male in providing parental care to the clutch. As this still increases the fitness of the conspecifics involved, it can still be seen as sexual selection.
Male zebra finches have been shown to selectively breed with females with a higher chance of laying a large clutch of eggs due to prior exposure to a high quality diet (Monaghan, 1996). This shows that in some species, the female individual's likelihood of obtaining a mate is directly correlated with her capacity to produce high quality clutches of eggs, independent of other factors such as age, body size or other characteristics.
It is not always only the males who show sexual traits, this definitely is the case for most species but there are some cases where the females of the species are equally or more ornamented than the males. Darwin (1871) recognised this and said about the matter:
"There are... exceptional cases in which the males, instead of having been selected, have been the selectors. We recognise such cases by the females having been rendered more highly ornamented than the males ..."
This can be explained either through genetic correlation of male sexual characteristics or the effects of direct selection (sexual or natural). This is explained well in a review by Amundsen (2000). Genetic correlation refers to the fact that the genome is mainly shared between the two sexes and hence sexual ornamentation in males may well be inherited by females. This will only be inhibited if a strong selective force acts to end the female ornamentation trait expression. The effects of direct selection involve the favouring of decorative female traits in a selective capacity. This may be related to either a sex role reversal whereby the males are the 'choosing' sex and females compete for the attention of male individuals, or in competition with other female individuals - in this case the ornamentation may be regarded as 'status badges', to show a female's place in the group hierarchy. The latter was coined 'social selection' by West-Eberhard (1983).
Female sexually selected traits can be confused with defence mechanisms, Illes & Yunes-Jimenez (2009) found that female stripe-headed sparrows (Aimophila r. ruficauda) out-sung male counterparts when they were subjected to a simulated territory intrusion by another sparrow. Birdsong is a large component in avian communication and mate-finding, while also being a deterrent to other birds for territory defence.
Doherty et al. (2003) found during a continental 21 year study that bird species under the influence of strong sexual selection (e.g. dichromatic birds) were, on average, 23% more likely to become extinct than monochromatic species (not under such heavy selective pressures). However the number of dichromatic species overall did not decrease over the study, this is because of the high turnover rate of dichromatic species, leading to a relatively stable community in general, i.e. extinctions were followed by new colonisations reasonably quickly.
The processes of sexual selection in birds has lead to higher speciation rates than in other groups of animals (Owens et al., 1999), this is most widespread in birds with promiscuous mating systems. Complex sexually selected behaviour can lead to higher rates of speciation due to the level of discrimination involved when choosing a partner, factors can include body size, shape, form or abilities, and can greatly influence which individuals have the highest fitness. Hence, differences can develop quickly between populations leading to high rates of speciation. This is supported by Seddon et al. (2008) who found a positive relationship between the intensity of sexual selection (in this case, birdsong in antbirds) and species diversity. There are contrasting views though, such as that of Morrow et al. (2003) who found that there was no overall correlation between sexual selection and species richness in birds, suggesting it may be positively correlated in some species, negatively correlated in some, and not correlated at all in others.
The prevailing explanation for the widely observed phenomenon that male individuals are larger than female conspecifics is that sexual selection selects for larger males. Karubian and Swaddle (2001) looked at a clade of Cardueline finches and found that it is often (approximately 50% of the time) due to a selective drive for decreased female size rather than increased male size that causes this sexual dimorphism to come about. This could be due to natural or sexual selection, or both. They suggest that any study looking at the selective forces driving sexual dimorphism "be tested on a case-by-case basis using a phylogenetic approach."
Sexual selection does not just occur on the external phenotypic features of birds, it can also arise post-insemination with sperm from several males competing to fertilise a single egg (Pizzari, 2007). Sexually selected sperm adaptations include "relatively large testes, large sperm stores and long spermatozoa, mate guarding and frequent pair copulations" (Birkhead, 1998), this study also finds that the most significant factor is the time of copulation - the male that deposits its sperm closest to the onset of oviposition. Sperm competition adds a further level of selection to reproduction, ensuring the offspring are of the highest genetic quality. Even after oviposition there are still sexually selected signals being given off, Soler et al. (2008) found that the colour of the egg in spotless starlings (Sturnus unicolor) was an indicator of the health of the female that laid the egg. When the researchers removed vital wing feathers from a female the intensity of the blue-green colouration on eggs she lay decreased; then they tried using artificial eggs with high blue-green colour intensities, this caused the paternal male to increase his feeding efforts significantly. This evidence supports the prediction that egg colour is an important sexually selected attribute.
Colour is a typical phenotypic quality looked at while studying sexual selection in birds, particularly in birds of paradise, which often have bright plumages to attract mates. However it is not often that simple, many bird species are able to see in the ultraviolet waveband (300-400nm) to which humans are blind to. Hunt et al. (1997) looked at the hypothesis that ultraviolet cues are used in avian mate-choice decisions, they found that ultraviolet signals played an important role in mate choice. When female zebra finches (Taeniopygia guttata) viewed a group of males, some wearing UV bands and some not, through a filter that allowed ultraviolet light through they tended to prefer those wearing the UV bands. When the filter was changed to block ultraviolet light there was no such preference. This was supported by another study by Bennett et al. (1996). This shows that some significant sexual signals may not be visible to us as humans. It also highlights the importance of careful experimental design, and meticulous research on observed animals.
There are some mechanisms of sexual selection that are slightly more abstract, Andersson (1996) suggested processes such as endurance rivalry, whereby a male is able to remain reproductively active for longer than other competing males. Other mechanisms include coercion (Clutton-Brock & Parker, 1995; Smuts & Smuts, 1993), which makes use of the same traits as male conflict contests (threatening behaviour, larger size, agility, better morphological 'weapons') to force copulation. Pradhan & Van Schaik (2009) found that females attempt to avoid coercive males in order to maximise fitness by relying on other male viability factors such as health and ornaments, this is because coercive males may not always be the most viable. In some species infanticide is even used as a method of sexual selection, killing off the offspring of competing males in order to increase one's own fitness (Andersson, 1996).
It is widely accepted that females use male ornamentation as a means of assessing a potential partner's fitness benefit to her offspring (Zahavi, 1975; Andersson 1996); however there is also evidence that concludes that females look for genetic diversity in their partners. There are certain benefits in having a partner that is genetically dissimilar, chances of beneficial mutations are higher and hence fitness could increase. The paradox of using absolute criteria (ornamentation) against relative criteria like genetic diversity is studied by Mays & Hill (2004); they found that there is evidence for mate choice based on genetic similarity in a restricted number of species, but recommend more research is needed in this field.
To conclude, it is evident that sexual selection plays a significant role in the evolution of many avian species. Birds are part of the class Aves which is an intensely studied group in regard to sexual selection; this is, in part, due to the large amount of sexual dimorphism that can be found typically in avian species. Research in this field has yet to find a universal theory or explanation concerning sexual selection in birds, and it is doubtful one will ever be found; the interactions between individuals participating in mate-choice decisions are far too complex to be described in simple terms, especially when allowing for discreet signals such as pheromones and ultraviolet colouration cues. All the theories and models discussed thus far must be taken into account when looking into this area.