University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln

Eileen Hebets Publications Papers in the Biological Sciences

2010

Mate Choice and Learning

Eileen Hebets University of Nebraska-Lincoln, [email protected]

Laura Sullivan-Beckers University of Nebraska-Lincoln, [email protected]

Follow this and additional works at: https://digitalcommons.unl.edu/bioscihebets

Part of the Behavior and Ethology Commons

Hebets, Eileen and Sullivan-Beckers, Laura, "Mate Choice and Learning" (2010). Eileen Hebets Publications. 46. https://digitalcommons.unl.edu/bioscihebets/46

This Article is brought to you for free and open access by the Papers in the Biological Sciences at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Eileen Hebets Publications by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. Published in Encyclopedia of Animal Behavior, edited by Michael D. Breed and Janice Moore. Amsterdam: Elsevier B.V., 2010, vol. 2, pp. 389-393. Copyright © 2010 Elsevier Ltd. Used by permission.

Mate Choice and Learning

E. A. Hebets and L. Sullivan-Beckers, University of Nebraska–Lincoln, Lincoln, NE, USA

Introduction choice learning. For example, the use of public informa- tion relieves an individual from personally gathering While an individual’s genetic framework is a major con- information and could minimize costs typically associ- tributor in determining its eventual mate choice, the role ated with mate assessment such as exposure to preda- of the environment in further influencing mating deci- tors or decreased time devoted to other important ac- sions has long been recognized. Animals gather informa- tivities such as foraging. Mate-choice learning more tion from the environment throughout life, and in some generally permits flexibility in mate choice, which could cases, may apply this information to increase their odds be extremely important in a changing environment. In of obtaining a high-quality mate. In short, these individu- the following text, examples of different forms of mate- als learn. Moreover, such learning can have a social com- choice learning will be provided and the state of re- ponent. “Social learning” is a general term that describes search in this area summarized. any learning based on observing, interacting with, and/ or imitating others in a social context. Social learning can Private (Personal) Information transmit information vertically, generation to generation (e.g., parent to offspring) and/or horizontally, within a Juvenile Experience: Mate-Choice Imprinting generation (as individual to individual). This form of in- formation transfer is generally referred to as “cultural “Mate-choice imprinting” refers to the learning process, transmission.” This entry will focus on social learning or processes, by which young individuals acquire - that relates to mate choice – mate-choice learning. ual preferences based on their observation of adults. Mate-choice learning can be separated into two broad Several specific forms of imprinting exist and -the gen categories: learning based on personal experiences with eral tenet was first described by Douglas Spalding in others (referred to as “private” or “personal informa- the nineteenth century as he recounted his observations tion”) or learning that results from the observation of of newly hatched chicks following random moving ob- others (referred to as “public information”). Learning jects. Despite its early description, however, the notion from private experiences can occur at the juvenile or of imprinting was not popularized until the 1930s by adult stage and may include encounters with conspe- the pioneering work of the Nobel Prize winning Aus- cifics or heterospecifics, same sex or opposite-sex indi- trian ethologist, Konrad Lorenz. Similar to other forms viduals (Figure 1). Mate-choice imprinting, for exam- of imprinting (e.g., filial imprinting), sexual imprinting, ple, demonstrates how an early experience based on or mate-choice imprinting, typically takes place during private information shapes subsequent mate choice. a sensitive period early in life. Historically, it has most Conversely, public information refers to any informa- frequently been observed in with parental care, tion gained through the observations of other individ- where the young use the parent of the opposite sex as ual’s experiences. An example of the use of public in- the model upon which they base their future mating formation is mate-choice copying, for example, when a preferences. This kind of early mate-choice imprinting female mimics the mating decision of another female in is thought to function to ensure conspecific matings, en- the population. Mate choice that is influenced by private abling individuals to avoid presumably costly hetero- information is sometimes termed “independent mate specific matings. Nonetheless, it is now clear that mate- choice,” whereas mate choice based on public informa- choice imprinting is not always restricted to an early tion is “nonindependent mate choice.” sensitive period and that preferences often continue to Mate-choice learning, whether it is through the acqui- be modified throughout development. sition of private or public information, balances various Crossfostering experiments are one of the primary costs and benefits. For example, the process of learning means by which scientists study early mate-choice im- itself can be costly, a topic covered in depth elsewhere. printing and such studies are most easily, and frequently, Additionally, costs can come in the form of imprinting conducted with . In crossfostering experiments, off- on the wrong species (which could lead to reduced fit- spring are raised by parents of either another ness), or from copying another individual that has cho- (e.g., a different color morph) or another species and, sen poorly itself. Nonetheless, the prevalence of mate- subsequently, their adult mate choice is examined. Us- choice learning across taxonomic groups suggests that ing crossfostering experiments, mate-choice imprinting there are significant benefits associated with mate- has been demonstrated in numerous species includ-

389 390 Hebets & Sullivan-Beckers in Encyclopedia of Animal Behavior (2010)

Figure 1. Mate-choice learning as influenced by social environment. This diagram depicts the various sources of social information that can impact mate-choice learning; the various life stages during which learning might be important; and some of the documented outcomes of mate-choice learning. Sections marked with “***” indicate topics for which research is lacking or nonexistent, and we suggest that these might be potentially fruitful areas for future focus. ing, but not confined to snow geese, zebra finches, Ben- mathematical models have been constructed to examine galese finches, great tits, blue tits, and red jungle fowl. In the various aspects of mate-choice imprinting. For ex- , reciprocal crossfostering of sheep and goats ample, population genetic models have been used to ex- has demonstrated a role of maternal imprinting on sub- plore the of different forms of imprinting. In sequent sexual preferences. Similarly, in Lake Victoria these models, Tramm and Servedio compared the evo- , females of some species appear to imprint on the lution of paternal, maternal, and oblique imprinting and phenotype of their mother. Crossfostering experiments found that paternal imprinting was the most likely to supporting a process of mate-choice imprinting are prev- evolve. Their results suggest that the success of a partic- alent, yet studies do exist for which such early experi- ular imprinting strategy is most influenced by the group ences have not influenced adult mate choice—raising in- of individuals that are imprinted upon (termed the “im- teresting questions about species-level differences in the printing set”). potential for, and importance of, mate-choice learning. Traditional examples of mate-choice imprinting, as Juvenile Experience: Mate Selectivity outlined earlier, are often restricted to species in which young spend significant time with their parents, thus, Mate-choice imprinting involves juvenile individuals enabling parental imprinting (either paternal or mater- imprinting on, or learning, various characteristics of nal). However, mate-choice learning may also be preva- an adult model, whether the model is their mother, fa- lent in species that lack parental care, yet still have sig- ther, or another nonparental adult. Subsequently, these nificant exposure to other conspecifics. For example, learned characteristics are incorporated into the indi- female wolf spiders are known to choose to mate with vidual’s mate-choice criteria, and mating partners with mature males of a phenotype with which they had expe- similar characteristics are preferred. However, experi- rience as a subadult. This type of imprinting is referred ence with conspecific adults may not always lead toa to as “oblique imprinting”—imprinting on a nonpa- preference for individuals resembling a model. Some- rental adult. In another example of oblique imprinting, times, early experience may simply increase choosiness. damselfly males alter their preference of female morphs Such effects of early experience have been documented based upon prior experience – males raised in the ab- in various animal taxa. For example, in both field crick- sence of females show no preference, while those raised ets and wolf spiders, research has shown that early ex- with one female form subsequently exhibited a prefer- perience by females with courtship songs or displays ence for females of that form. Planthoppers have also can lead to increased selectivity for mates. been shown to exhibit a learned preference for conspe- cifics. Finally, in humans for whom arranged marriages Adult Experience: Mate Selectivity are the norm, the experiences young women have out- side the traditional family environment, including expo- Effects of experience on mate choice need not be re- sure to outside media and participation in youth groups, stricted to young or immature individuals. As adults, influence their involvement in marriage arrangements. encounters with rivals and potential mates can also alter In addition to empirical studies that utilize crossfos- mating behaviors for both males and females. For exam- tering or various early exposure techniques, numerous ple, in some spiders, fruit flies, crickets, and newts, na- Mate Choice and Learning 391 ive females are less discriminating in mate choice than ment between sources of information available to a older and more experienced females. A female’s thresh- female may determine when a female copies mating de- old to accept a male can also change with successive en- cisions and when she will forego mate-choice copying, counters, both pre- and post-mating. Presumably, as relying instead on private assessment. In some species, females gain experience with mates, they learn to dis- when public and private information conflict, females tinguish among them. A significant literature exists on base decisions on their own assessment, while in other female search strategies (e.g., sequential search, best-of- species, females revert to mate-choice copying in such n, and variable threshold), many of which implicitly as- situations. In humans, mate-choice copying has been sume learning. documented to depend on the quality of the model fe- Not only do adult females alter their mate choice male observed with a potential mate. Additionally, in based upon their personal experiences with mature humans as well as other taxa, the degree to which fe- males, but they may also alter their preferences based males will copy mating decisions of others is influenced on personal information regarding their own attractive- by sexual experience. In many cases, virgin females are ness. In humans, for example, attractive females have more likely to copy mate-choice decisions than more stronger preferences for high-quality males than less at- sexually experienced females. Mate-choice copying has tractive females, and in zebra finches, a female’s self- been documented in vertebrate (e.g., , birds, and perception has been shown to influence her mate choice. mammals) and invertebrate (e.g., insects) species. In nature, this self-assessment may or may not be learned, but theoretical models suggest that the percep- Mechanisms of Mate-Choice Learning tion of one’s own attractiveness could develop through previous experiences with the opposite sex, resulting in Identifying and describing the physiological mecha- increased choosiness following successful encounters nisms that underlie the relationship between learning and decreased choosiness following rejection by poten- and mate choice is a vast area of research. Here, some tial partners. of the major findings of the field are summarized. The Thus far, we have been focusing mostly upon fe- neurophysiology of early mate-choice imprinting in ze- male mating preferences. However, males have also bra finches has been extensively explored. -Immedi been shown to alter mating behaviors with experience. ate-early (c-fos and ZENK) have been used to es- As males are rejected or accepted by females, they may timate neuronal activity and to identify activated brain become more or less sexually aggressive and/or more regions with exposure to novel and previously experi- or less discriminating. Trinidad males, for exam- enced stimuli. Researchers have also investigated neu- ple, learned to direct courtship at conspecific females af- ronal control of the length and timing of the sensitive ter 4 days of contact with conspecific and heterospecific period for sexual imprinting. In , the neuro- females. In damselflies, males prefer females of a morph sensory pathway that functions in the male and female with which they have had previous experience. In Dro- brain to determine whether to attempt courtship with a sophila, a male’s experience with a heterospecific female potential mate based on previous experience, has been often leads to reduced future courtship effort toward described. In mice, after investigating the volatile chem- heterospecific females. In wolf spiders, previous mate ical signals present in female urine, males acquire more effects are known to shape a male’s future mating suc- complex and extensive preferences for the of sex- cess. Males that had experienced, but not mated with, ually receptive females. These male preferences cor- a female were less likely to mate in the next encounter. respond to changes in the piriform cortex of the brain, However, if the male had mated with the previous fe- and knockout studies have demonstrated that the male, it was more likely to mate with the next. Peg3 disrupts these effects of experience. Thus, in dispa- rate taxonomic groups, significant information is avail- Public Information able on the physiological mechanisms underlying mat- ing choice learning, and this remains an active area of Adult Experience: Mate-Choice Copying research.

In various taxa (although primarily in fish and birds), Evolutionary Consequences of Mate-Choice females observe and copy the mating decisions of con- Learning specific females. In some cases, mate-choice copying leads to an increased preference for the male traits ob- One of the most intriguing and intellectually stimulating served in the mated male. In other cases, females may aspects of mate-choice learning is its potential to drive prefer the actual male that was observed mating with evolutionary change. Not surprisingly then, exploring another female. Mate-choice copying has the benefit of the evolutionary consequences of mate-choice learning decreasing the investment in mate assessment that a fe- is an extremely active area of research, rich with theory male must make. The reliability, consistency, and agree- and modeling. The most frequently discussed aspects of 392 Hebets & Sullivan-Beckers in Encyclopedia of Animal Behavior (2010) mate-choice learning involve its putative influence on for both males and females, could facilitate conspecific such evolutionary processes as , hybridiza- matings. Indeed, in whydahs and indigobirds (interspe- tion, and . cific brood parasites in the genus Vidua), parasitic male offspring copy the song of their foster fathers. Parasitic Speciation and Mate-Choice Learning female offspring also imprint on their foster father’s song. This host imprinting ultimately enables parasitic It has frequently been suggested that mate-choice im- offspring to find conspecific mates as adults. This pro- printing can facilitate . Imprinting cess of host imprinting has been proposed as a mecha- on one’s parental phenotype, for example, leads to posi- nism promoting diversification in this group, as host tive , where similar pref- shifts could readily lead to reproductive isolation. How- erentially mate with each other. Any new phenotype, or ever, one could also imagine a scenario where mate- novel trait, appearing in a population could rapidly lead choice imprinting on a host could lead to hybridization. to reproductive isolation via mate-choice imprinting, For example, if numerous species utilize the same host, even if it is initially present at a low frequency. Empiri- the likelihood of parasitic individuals mating with a het- cal work with collared flycatchers (Ficedula albicollis) has erospecific brood parasite increases, and recent work provided support for such a mechanism, as the artifi- has indicated that continued does exist be- cial introduction of a novel trait (a red stripe on a male’s tween some host races. forehead) led to positive assortative mating – females having experienced males with a red stripe were more Hybridization and Mate-Choice Learning likely to pair with males possessing red stripes. The ini- tial effects of such mate-choice imprinting could then be Although mate-choice imprinting often results in posi- followed by . In fact, a recent mathe- tive assortative mating, typically with conspecifics, the matical model has demonstrated that reinforcement (en- potential exists for misimprinting, or imprinting on the hancement of premating isolation) can occur via learned wrong species. Hybridization between species of Dar- mating preferences. It is important to note, however, win’s finches, for example, is known to occur and is that the influence of mate-choice imprinting on evolu- thought to result from misimprinting. Additionally, tionary processes such as speciation depends implic- crossfostering experiments conducted in the wild have itly upon the imprinting set, or the individuals used as demonstrated that some bird species will imprint on a models. For example, imprinting on a nonparental phe- foster parent of another species, resulting in heterospe- notype (oblique imprinting such as mate-choice copy- cific pairings. ing) would likely inhibit population divergence. None- Heterospecific matings could result in hybrid off- theless, the involvement of mate-choice imprinting on spring and hybrid zones are not uncommon in nature. speciation and diversification has likely been important What role then, if any, does mate-choice imprinting for numerous taxonomic groups and has been explicitly play in hybrid zones? Using an artificial neural -net suggested to have played a role in the diversification of work, Brodin and Haas demonstrated that phenotypes various birds (e.g., Galapagos finches; various brood of pure species are learned faster and better than those parasites) as well as fishes (e.g., Lake Victoria cichlids). of hybrids, potentially leading to selection against hy- The occurrence of interspecific brood brids. Further spatial simulations combined with em- raises unique questions with respect to the evolution- pirical data on dispersal demonstrate that mate-choice ary implications of mate-choice imprinting. Conse- imprinting can maintain a hybrid zone under natural quently, a significant amount of research addresses the conditions. role of mate-choice imprinting on speciation and diver- sification in avian brood parasites. Interspecific brood Sexual Selection and Mate-Choice Learning parasites constitute approximately 1% of all bird spe- cies and are defined as those species for which adults In addition to its role in speciation and hybridization, do not care for their young, but instead deposit their mate-choice learning might also lead to the evolutionary eggs in the nests of other species, where the young are change of specific traits within a species, especially traits left to be raised by foster parents. Given the common that are sexually selected. For example, mate-choice im- occurrence of mate-choice imprinting in birds, an obvi- printing can lead to sexual preferences for extreme phe- ous question arises regarding how imprinting on a fos- notypes beyond which an individual has experienced, ter parent might influence subsequent reproductive suc- potentially driving trait elaboration. One mechanism cess of the parasitic offspring. For example, if parasitic by which this is possible is via peak shift – a conse- offspring imprint on visual aspects of their foster par- quence of discrimination learning of differentially re- ent, their subsequent ability to find a conspecific mate inforced stimuli (e.g., individuals are trained such that could be severely compromised. However, imprinting one stimulus is rewarded and the other is punished). Es- on the song of the foster parent (which can be learned), sentially, peak shift can lead to a preference for an ex- Mate Choice and Learning 393 aggerated trait never previously experienced. For ex- See also: Alex: A Study in Avian Cognition; Apes: Social Learning; ample, in an elegant study using zebra finches, ten Cate Avian Social Learning; Behavioral Ecology and Sociobiology; Collec- and colleagues raised males with the parents of artifi- tive ; Costs of Learning; Cultural Inheritance of Signals; cially painted beaks (orange or red). In subsequent mat- Culture; Decision-Making: Foraging; Fish Social Learning; Flexible Mate Choice; Imitation: Cognitive Implications; Insect Social Learn- ing trials, they were able to show a shift in male beak ing; Isolating Mechanisms and Speciation; Learning and Conservation; color preference, with males directing more courtship Mammalian Social Learning: Non-Primates; Mate Choice in Males to females at the extreme maternal end of the spectrum, and Females; Memory, Learning, Hormones and Behavior; Monkeys despite the fact that this beak color was more extreme and Prosimians: Social Learning; Psychology of Animals; Sexual Selec- than seen in the model parent. tion and Speciation; Social Cognition and Theory of Mind; Social In- The above-mentioned example addresses the role formation Use; Social Learning: Theory; Vocal Learning. of parental imprinting on trait evolution. However, oblique imprinting, or imprinting on a nonparental adult, also has intriguing potential regarding the evo- Further Reading lution of secondary sexual traits. The cultural trans- mission of mating preferences, or passing on of mating Bischof H-J and Rollenhagen A (1998) Behavioral and neurophysio- preferences through nongenetic mechanisms, could lead logical aspects of sexual imprinting in zebra finches. Behavioral to evolutionary changes in secondary sexual traits, or Brain Research 98: 267–276. cultural inheritance. Cultural transmission refers to the Drullion D and Dubois F (2008) Mate-choice copying by female ze- bra finches, Taeniopygia guttata: What happens when model fe- process by which the phenotype of a species can change males provide inconsistent information? Behavioral Ecology and based upon information acquired during an individu- Sociobiology 63: 269–276. al’s lifetime. Essentially, the cultural transmission of fe- Dukas R (2005) Learning affects mate choice in female fruit flies. Be- male preferences (via juvenile experience effects with havioral Ecology 16: 800–804. nonparental adult conspecifics or via mate-choice copy- Fawcett TW and Bleay C (2009) Previous experiences shape adap- ing) could drive the cultural inheritance of male sec- tive mate preferences. Behavioral Ecology 20: 68–78. ondary sexual traits. The details of such evolutionary Hebets EA (2003) Subadult experience influences adult mate choice change would depend explicitly on the form of imprint- in an arthropod: Exposed female wolf spiders prefer males of a ing and on the imprinting set. familiar phenotype. Proceedings of the National Academy of Sciences of the United States of America 100: 13390–13395. Genotype-by-Environment Interactions and Mate- Immelmann K (1972) Sexual selection and other long-term aspects Choice Learning of imprinting in birds and other species. Advances in the Study of Behavior 4: 147–174. Thus far, we have focused solely on various environ- Irwin DE and Price T (1999) Sexual imprinting, learning and specia- mental effects on mate-choice learning, with no discus- tion. Heredity 82: 347–354. sion of the underlying . Yet, all organisms are Mery F, Varela SAM, Danchin E, et al. (2009) Public versus personal influenced by both their genes and their environment. information for mate copying in an invertebrate. Current Biology Much recent work has been directed explicitly at under- 19: 730–734. standing the interactions between an individual’s gen- Ophir AG and Galef BG (2004) Sexual experience can affect otype and its environment. Genotype-by-environment use of public information in mate choice. Animal Behavior 68: interactions (GEIs) have become one of the major ex- 1221–1227. planations regarding the maintenance of genetic varia- Qvarnstrom A, Blomgren V, Wiley C, and Svedin N (2004) Female tion in secondary sexual traits, despite putatively strong collared flycatchers learn to prefer males with an artificial novel ornament. Behavioral Ecology 15: 543–548. sexual selection that should diminish this variation. Servedio MR, Saether SA, and Saetre GP (2009) Reinforcement and While most studies of GEIs have focused on male sig- learning. Evolutionary Ecology 23: 109–123. naling traits, it seems equally likely that female prefer- Sirot E (2001) Mate-choice copying by females: The advantages of a ences are influenced by GEIs. For example, a female’s prudent strategy. Journal of Evolutionary Biology 14: 418–423. genotype may impact her likelihood and/or her ability Slagsvold T, Hansen BT, Johannessen LE, and Lifjeld JT (2002) Mate to learn mating preferences. Such GEIs with respect to choice and imprinting in birds studied by cross-fostering in the mate-choice learning would certainly influence the in- wild. Proceedings of the Royal Society of London Series B: Biological teractions between learned mate choice and the evolu- Sciences 269: 1449–1455. tion of male secondary sexual traits. Future work ex- ten Cate C, Verzijden MN, and Etman E (2006) Sexual imprinting can ploring the interactions between genotypes and social induce sexual preferences for exaggerated parental traits. Cur- environments will surely provide a rich source of new rent Biology 16: 1128–1132. knowledge and insights regarding mate-choice learning Tramm NA and Servedio MR (2008) Evolution of mate-choice im- and its role in evolutionary processes. printing: Competing strategies. Evolution 62: 1991–2003