Sexual Imprinting

Sexual imprinting is the process by which young animals learn a sexual preference for opposite sex conspecifics. The effects of this early learning process become manifest in adult mate choice. The social parents usually serve as templates for the young in the establishment of the mate preference. There is also some evidence that siblings may influence the development of mate recognition.

Most research on sexual imprinting has been performed with birds. Among birds, sexual imprinting has been documented in more than 100 species and seems to be the rule rather than the exception. Sexual imprinting has also been documented among mammals and fish. It is not limited to rapidly evolving species, or males only, as has been suggested. Most studies on sexual imprinting have been performed in a laboratory setting, particularly with zebra finches, mallards, and quail. However, the existing field studies show that sexual imprinting is also prevalent under natural conditions, and generally confirm the properties of the learning process as they have been documented in the laboratory.

Typical experiments demonstrating sexual imprinting involve some kind of manipulation of the parental phe-notype. Interspecific cross-fostering is frequently used, that is, the experimenters let young of one species be reared by adults of another species. The result of this treatment is usually that cross-fostered individuals express a sexual preference for their foster species when tested in mate choice trials as adults (Figure 1). This is proof that mate choice is learned, since normally reared individuals do not express any preference for heterospe-cifics. Similarly, young raised by parents with an artificial ornament may learn a preference for this ornament.

Previously it was thought that sexual imprinting was confined to a short period early in life. However, a series of laboratory experiments on the zebra finch showed that this notion was incomplete, and redefined the understanding of the sensitive period and the irreversibility of sexual imprinting. They showed that birds raised by het-erospecific foster parents develop a preference for their foster species if they also experience their first courtship

Figure 1 A blue tit female paired to a great tit male, feeding young. Blue tits raised by great tits and great tits raised by blue tits imprint sexually on their foster species. Heterospecific couples may be formed between such interspecifically cross-fostered individuals. Photo copyright: Tore Slagsvold.

Figure 1 A blue tit female paired to a great tit male, feeding young. Blue tits raised by great tits and great tits raised by blue tits imprint sexually on their foster species. Heterospecific couples may be formed between such interspecifically cross-fostered individuals. Photo copyright: Tore Slagsvold.

with that foster species. However, if such cross-fostered birds are exposed to conspecifics during first courtship or breeding, they may shift their initial preference toward conspecifics. These findings have been corroborated by studies of the zebra finch forebrain where physical changes accompany the early experiences as well as the experiences during first courtship. It thus seems like sexual imprinting is accomplished in two separate stages.

Several studies have documented that interspecifically cross-fostered individuals in species that do show sexual imprinting may also have a sexual preference for conspe-cifics in spite of the experience of having been raised by heterospecifics. There are several potential sources for such an own-species bias. First, the bias may be genetically encoded, that is, mate recognition may to some extent be inherited rather than learned. Second, an own-species bias may have arisen as a result of conspecifics initiating more courtship than do heterospecifics toward the interspecifically cross-fostered individuals. Hence, the behavior of the stimulus individuals in the experimental mate choice situation may influence and even constrain the mate choice of the cross-fostered individuals. Third, factors such as the amount of care received by the parents, or the number of siblings in the nest, may influence the degree of imprinting, and such factors may have differed between cross-fostered and control individuals. In sum, there are many potential sources of variation in the development of mate choice. These must be kept in mind when designing and drawing conclusions from experiments on imprinting.

Some studies have revealed that the recognition of same-sex individuals also may be influenced by imprinting. Interspecifically cross-fostered great tits and blue tits respond aggressively toward same-sex individuals of their heterospecific foster species during the breeding season, while normally reared controls of both species respond aggressively only toward conspecifics. This effect lasts for life (Figure 2). It is not known whether the development of such rival recognition is different from sexual imprinting. However, the fact that the appearance of rivals also may be learned highlights the function of imprinting in the development of species recognition as a whole.

Species recognition is a prerequisite for adequate mate choice, and learning species-specific characteristics from social parents and/or siblings is reliable because social parents and offspring are usually of the same species. A notable exception is the case of interspecific brood parasites such as cuckoos and cowbirds, which leave their young to be reared in nests of heterospecifics. Initially, it was thought that recognition templates were genetically inherited in brood parasites. However, recent findings suggest that the early social environment affects choices of social partners and mates in some brood-parasitic species. The timing of learning may have been shifted to the

Age (years)

Figure 2 Rival imprinting in blue tits persists with age. Aggressive response ratio (y-axis) is measured as the aggressive response toward blue tits divided by the sum of the aggressive responses toward blue tit and great tit intruders into the territory. Hence, a ratio of 50% means equal responses to great tits and blue tits, while a higher ratio means a stronger relative response toward blue tits than great tits. Control blue tits (triangles) respond mostly toward blue tit intruders into their territory, while blue tits cross-fostered to great tits (circles) respond aggressively toward both great tit and blue tit intruders, and this pattern persists throughout the life span of the respondents. Aggressive response is measured as the proportion of 5 min spent within 2 m of a caged intruder placed near the nest box of breeding respondents. All respondents were sequentially presented with individuals of both species. Symbols indicate arithmetic means ± SE. Reproduced from Hansen BT, Johannessen LE, and Slagsvold T (in press) Imprinted species recognition lasts for life in free-living great tits and blue tits. Animal Behaviour (doi:10.1016/j.anbehav.2007.07.023; available online 29 Oct. 2007), with permission from Elsevier.

postfledgling stage for species that do not associate with conspecifics earlier. It has been suggested that conspecific recognition in the obligately brood-parasitic brown-headed cowbird is initiated when a young brood parasite encounters an innate species-specific vocalization that triggers learning of additional aspects of the vocalizing individual's phenotype.

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