The neural mechanisms of mate choice: a hypothesis

Scientists have described many physical and behavioral traits in avian and mammalian species that evolved to attract mates. But the brain mechanisms by which conspecifics become attracted to these traits is unknown. This paper maintains that two aspects of mate choice evolved in tandem: 1) traits that evolved in the "display producer" to attract mates and, 2) corresponding neural mechanisms in the "display chooser" that enable them to become attracted to these display traits. Then it discusses our (in-progress) fMRI brain scanning project on human romantic attraction, what we believe is a developed form of "courtship attraction" common to avian and mammalian species as well as the primary neural mechanism underlying avian and mammalian mate choice. The paper hypothesizes that courtship attraction is associated with elevated levels of central dopamine and norepinephrine and decreased levels of central serotonin in reward pathways of the brain. It also proposes that courtship attraction is part of a triune brain system for mating, reproduction and parenting. 1)The sex drive evolved to motivate birds and mammals to court any conspecifics. 2) The attraction system evolved to enable individuals to discriminate among potential mating partners and focus courtship activities on particular individuals, thereby conserving mating time and energy. 3) The neural circuitry for attachment evolved to enable individuals to complete species-specific parental duties.     

Romantic love: a mammalian brain system for mate choice

Mammals and birds regularly express mate preferences and make mate choices. Data on mate choice among mammals suggest that this behavioural 'attraction system' is associated with dopaminergic reward pathways in the brain. It has been proposed that intense romantic love, a human cross-cultural universal, is a developed form of this attraction system. To begin to determine the neural mechanisms associated with romantic attraction in humans, we used functional magnetic resonance imaging (fMRI) to study 17 people who were intensely 'in love'. Activation specific to the beloved occurred in the brainstem right ventral tegmental area and right postero-dorsal body of the caudate nucleus. These and other results suggest that dopaminergic reward and motivation pathways contribute to aspects of romantic love. We also used fMRI to study 15 men and women who had just been rejected in love. Preliminary analysis showed activity specific to the beloved in related regions of the reward system associated with monetary gambling for uncertain large gains and losses, and in regions of the lateral orbitofrontal cortex associated with theory of mind, obsessive/compulsive behaviours and controlling anger. These data contribute to our view that romantic love is one of the three primary brain systems that evolved in avian and mammalian species to direct reproduction. The sex drive evolved to motivate individuals to seek a range of mating partners; attraction evolved to motivate individuals to prefer and pursue specific partners; and attachment evolved to motivate individuals to remain together long enough to complete species-specific parenting duties. These three behavioural repertoires appear to be based on brain systems that are largely distinct yet interrelated, and they interact in specific ways to orchestrate reproduction, using both hormones and monoamines. Romantic attraction in humans and its antecedent in other mammalian species play a primary role: this neural mechanism motivates individuals to focus their courtship energy on specific others, thereby conserving valuable time and metabolic energy, and facilitating mate choice.     

Simultaneously hermaphroditic shrimp use lipophilic cuticular hydrocarbons as contact sex pheromones

Successful mating is essentially a consequence of making the right choices at the correct time. Animals use specific strategies to gain information about a potential mate, which is then applied to decision-making processes. Amongst the many informative signals, odor cues such as sex pheromones play important ecological roles in coordinating mating behavior, enabling mate and kin recognition, qualifying mate choice, and preventing gene exchange among individuals from different populations and species. Despite overwhelming behavioral evidence, the chemical identity of most cues used in aquatic organisms remains unknown and their impact and omnipresence have not been fully recognized. In many crustaceans, including lobsters and shrimps, reproduction happens through a cascade of events ranging from initial attraction to formation of a mating pair eventually leading to mating. We examined the hypothesis that contact pheromones on the female body surface of the hermaphroditic shrimp Lysmata boggessi are of lipophilic nature, and resemble insect cuticular hydrocarbon contact cues. Via chemical analyses and behavioural assays, we show that newly molted euhermaphrodite-phase shrimp contain a bouquet of odor compounds. Of these, (Z)-9-octadecenamide is the key odor with hexadecanamide and methyl linoleate enhancing the bioactivity of the pheromone blend. Our results show that in aquatic systems lipophilic, cuticular hydrocarbon contact sex pheromones exist; this raises questions on how hydrocarbon contact signals evolved and how widespread these are in the marine environment.     

The mating system of the White-throated Magpie-jay Calocitta formosa and Greenwood's hypothesis for sex-biased dispersal

Greenwood explained the different sex bias in dispersal of birds (usually female biased) and mammals (usually male biased) by a difference in mating systems: male birds primarily defend resources while male mammals primarily defend females. The White-throated Magpie-jay Calocitta formosa is unusual among birds in that females are philopatric and jointly defend permanent resource territories while males disperse before they are 2 years of age. One female in a group is the primary breeder. One male joins the group permanently as her mate. Males that do not have a permanent breeding position circulate among groups and attempt to mate with both the primary breeding female and other group females. Other females feed the primary breeder and her offspring and also pursue other reproductive behaviour, including secondary nesting in the territory and egg dumping into the primary breeder's nest. I argue that the unusual dispersal pattern in this species is a result of the alternative reproductive strategies that can be pursued by males and females excluded from being primary breeders. The White-throated Magpie-jay conforms to Greenwood's predictions: males pursue a mate defence rather than resource defence mating system and they are the dispersing sex. The primary factor influencing alternative reproductive tactics may be asynchronous reproduction among groups during the long breeding season arising from frequent renesting in an area of high nest predation.     

Genetic compatibility, mate choice and patterns of parentage: invited review

There is growing interest in the possibility that genetic compatibility may drive mate choice, including gamete choice, particularly from the perspective of understanding why females frequently mate with more than one male. Mate choice for compatibility differs from other forms of choice for genetic benefits (such as 'good genes') because individuals are expected to differ in their mate preferences, changing the evolutionary dynamics of sexual selection. Recent experiments designed to investigate genetic benefits of polyandry suggest that mate choice on the basis of genetic compatibility may be widespread. However, in most systems the mechanisms responsible for variation in compatibility are unknown. We review potential sources of variation in genetic compatibility and whether there is any evidence for mate choice driven by these factors. Selfish genetic elements appear to have the potential to drive mate compatibility mate choice, though as yet there is only one convincing example. There is abundant evidence for assortative mating between populations in hybrid zones, but very few examples where this is clearly a result of selection against mating with genetically less compatible individuals. There are also numerous cases of inbreeding avoidance, but little evidence that mate choice or differential fertilization success driven by genetic compatibility occurs between unrelated individuals. The exceptions to this are a handful of situations where both the alleles causing incompatibility and the alleles involved in mate choice are located in a chromosome region where recombination is suppressed. As yet there are only a few potential sources of genetic compatibility which have clearly been shown to drive mate choice. This may reflect limitations in the potential for the evolution of mate choice for genetic compatibility within populations, although the most promising sources of such incompatibilities have received relatively little research.     

The evolution of female mate choice by sexual conflict

Although empirical evidence has shown that many male traits have evolved via sexual selection by female mate choice, our understanding of the adaptive value of female mating preferences is still very incomplete. It has recently been suggested that female mate choice may result from females evolving resistance rather than attraction to males, but this has been disputed. Here, we develop a quantitative genetic model showing that sexual conflict over mating indeed results in the joint evolution of costly female mate choice and exaggerated male traits under a wide range of circumstances. In contrast to tradition explanations of costly female mate choice, which rely on indirect genetic benefits, our model shows that mate choice can be generated as a side-effect of females evolving to reduce the direct costs of mating.     

Reproductive Behavior of Female Propithecus verreauxi at Beza Mahafaly,Madagascar

Prosimian and anthropoid females are generally thought to have divergent reproductive patterns, characterized by circumscribed and situation-dependent receptivity. This dichotomy underpins the traditional view that nonreproductive mating serves a social function in anthropoid females, distinguishing them from prosimians which, like most other mammals, mate only when conception is most probable. Circumscribed estrous cycles differ from anthropoid menstrual cycles by the presence of menstruation, and greater flexibility in timing and longer duration of receptivity in the latter. The degree to which sexual behavior is tightly synchronized to periovulatory events in Propithecus verreauxi was assessed via the behavioral, hormonal, and social correlates of reproduction in a free-ranging population. I collected data from two social groups before and during the 1990–1991 and 1991–1992 breeding seasons at Beza Mahafaly, Madagascar. I also conducted 644 focal-animal hours and collected 485 fecal samples from five marked females in the Vaovao and Vavy Masiaka social groups. Estrus was behaviorally characterized by 0.5–96-h periods of receptivity when females were motivated and willing to mate, the latter not always coincident with periovulatory events. Females exhibited age- and rank-related asynchronous receptivity, and in some cases, periovulatory synchrony within groups. Sifaka were not pair-bonded. Most females mated with multiple males, temporally ordering partners based on male residence and age. Mating was limited by male mate-guarding and sexual aggression by males, female mate competition, and aversions to mating with certain partners. It was facilitated by surreptitious copulations, positive mate choice, and the availability of non-resident mating partners.     

Calling,Courtship, and Condition in the Fall Field Cricket,Gryllus pennsylvanicus

Theoretically, sexual signals should provide honest information about mating benefits and many sexually reproducing species use honest signals when signalling to potential mates. Male crickets produce two types of acoustic mating signals: a long-distance mate attraction call and a short-range courtship call. We tested whether wild-caught fall field cricket (Gryllus pennsylvanicus) males in high condition (high residual mass or large body size) produce higher effort calls (in support of the honest signalling hypothesis). We also tested an alternative hypothesis, whether low condition males produce higher effort calls (in support of the terminal investment hypothesis). Several components of long-distance mate attraction calls honestly reflected male body size, with larger males producing louder mate attraction calls at lower carrier frequencies. Long-distance mate attraction chirp rate dishonestly signalled body size, with small males producing faster chirp rates. Short-range courtship calls dishonestly reflected male residual mass, as chirp rate and pulse rate were best explained by a curvilinear function of residual mass. By producing long-distance mate attraction calls and courtship calls with similar or higher effort compared to high condition males, low condition males (low residual mass or small body size) may increase their effort in current reproductive success at the expense of their future reproductive success, suggesting that not all sexual signals are honest.     

Chemical communication and mate attraction in echinostomes

Mate attraction is widespread among animals and appears to facilitate mating and to prevent hybridisation between closely related species. In this study we investigated mate preference between two geographical isolates of Echinostoma caproni (Trematoda, Platyhelminth) and another species of the genus Echinostoma E. sp. Because previous experiments showed a partial reproductive isolation between echinostome isolates, we examined the possibility that such isolation resulted from differential mate attraction. We compared intra-isolate, inter-isolate and interspecific pairings using two in vitro experimental designs. In the first experiment we compared mate attraction of two individuals belonging to or not belonging to the same isolate, while in the second experiment we examined mate choice when individuals were in the presence of individuals from both the same isolate and from a different isolate or a different species. Distances between worms were measured over a period of 90 min. Results from both experiments suggested that mate attraction was similar for intra-isolate, inter-isolate or interspecific combinations. This lack of mate preference in vitro would therefore support an alternative hypothesis of a reproductive isolation through sperm selection.     

Territoriality and Male Mating Success in the Dart-poison Frog,Epipedobates femoralis (Dendrobatidae,Anura)

The social and reproductive behaviour of the dart-poison frog, Epipedobates femoralis, was studied in Amazonian Peru for 14 months. Males defended territories with advertisement calls and, ultimately, fighting. Territory size ranged from 0.25 to 26 m² and was positively correlated with duration of residence and calling activity of the owner. Females were not territorial and were never attacked when approaching calling males. Males and females only mated once and females sampled calling males before mating. Male mating success was closely correlated with territory size and calling activity. No correlation was found between male body size and mating success. Territories provide residents with sufficient space for mate attraction and reproduction without interference from rivals. Since territory size is dependent on calling activity which involves high energetic costs, it is suggested that territory size reveals male quality.     

Is Self‐Grooming by Male Prairie Voles a Predictor of Mate Choice?

Self-grooming by mammals is a form of scent dissemination in which individuals anoint themselves with salivary, anogenital, and other body odours. Self-grooming has been proposed to be a sexually selected trait favoured in reproductive competition and sexual attraction. We tested the hypothesis that females would show a mating preference for males that self-groomed more than a reproductive competitor that groomed less. In mate-choice experiments in which females had a choice of two tethered males, non pair-bonded females did not choose males based on their frequency of self-grooming. In a second experiment in which pair-bonded females in postpartum oestrus had access to their current mate and two strange males, strange males groomed significantly more than pair-bonded mates, yet attained the fewest copulations. Non pair-bonded females and pair-bonded males and females groomed significantly less often than did non pair-bonded males. Self-grooming behaviour was consistent with the sexual attraction hypothesis, but the frequency of self-grooming did not increase a male's mating success. We conclude that the frequency and time spent self grooming are not good predictors of mating success.     

Behavioral characterization of attractin,a water-borne peptide pheromone in the genus aplysia

Pheromones play a significant role in coordinating reproductive activity in many animals, including opisthobranch molluscs of the genus APLYSIA: Although solitary during most of the year, these simultaneous hermaphrodites gather into breeding aggregations during the reproductive season. The aggregations contain both mating and egg-laying animals and are associated with masses of egg cordons. The egg cordons are a source of pheromones that attract other Aplysia to the area, reduce their latency to mating, and induce egg laying. One of these water-borne egg cordon pheromones ("attractin") has been characterized and shown to be attractive in T-maze assays. Attractin is the first water-borne peptide pheromone characterized in invertebrates. In the current studies, behavioral assays were used to better characterize the attraction, and to examine whether attractin can induce mating. Although the two activities could be related (i.e., attraction occurring because animals were looking for a partner), this was not tested. T-maze assays showed that attractin works as part of a bouquet of odors: the peptide is attractive only when Aplysia brasiliana is part of the stimulus. The animal does not need to be a conspecific, perhaps explaining why multiple species may be associated with one aggregation. Native and recombinant attractin are equally attractive, verifying that N-glycosylation at residue 8 is not required for attraction. Mating studies showed that both native and recombinant attractin reduce the latency to mating. The effects are larger when hermaphroditic mating is considered: in addition to reducing latency, attractin doubles the number of pairs mating as hermaphrodites. The effect may result from attractin stimulating both animals to mate as males and would be consistent with behaviors previously seen in the T-maze. Attractin may thus be contributing to the formation of copulatory chains and rings seen in aggregations in the field. These results may be interpreted in two ways: (1). attractin has multiple activities that contribute to the establishment and maintenance of the aggregation; or (2). the induced desire to mate may make attractin attractive when it is presented in conjunction with an animal. In either case, the results open the door for cellular and molecular studies of mechanism of action.     

Mating behavior of an aphidophagous ladybird beetle,Propylea dissecta （Mulsant）

Abstract The mating behavior of Propylea dissecta (Mulsant) was investigated in detail. Protandry was evident, as males mature earlier than females. Predicted age of sexual maturation of male and female ladybirds was 7.12 and 9.33 days, respectively. Males performed courtship in six steps, viz. approach, watch, examine, embrace, mount and attempt. Embrace is possibly an appeasement act, while examine serves to recognize mate. Chemical signals initiate male attraction toward females. Visual and tactile cues appear to secondarily help in mate recognition. Mating lasted longest (275.40±12.23 min) when it occurred between unmated individuals. It was much shorter (176.60±5.60 min) when prior mated individuals copulated. There was a significant decrease in mating durations when adults were subjected to five successive matings. Fecundity and percent egg viability increased significantly with increase in the number of matings.     

Assortative mating for relatedness in a large naturally occurring population of Drosophila melanogaster

New theoretical work on kin selection and inclusive fitness benefits predicts that individuals will sometimes choose close or intermediate relatives as mates to maximize their fitness. However, empirical examples supporting such predictions are rare. In this study, we look for such evidence in a natural population of Drosophila melanogaster. We compared mating and nonmating individuals to test whether mating was nonrandom with respect to relatedness. Consistent with optimal inbreeding, males were more closely related to their mate than to randomly sampled females. However, all individuals collected mating showed higher relatedness and males were not significantly more related to their mate than to other mating females. We also found a negative relationship between relatedness and fecundity. Our results are consistent with the hypothesis that inclusive fitness benefits may drive inbreeding tolerance despite direct costs to fitness; however, an experimental approach is needed to investigate the link between mate preference and relatedness.     

Reproductive strategies of rhesus macaques

Reproductive strategies incorporate a multitude of mechanisms that have evolved to promote the reproductive success of individuals. Evolutionary perspectives tend to emphasize the advantages of male-male competition and female choice as mediators of differential reproduction. Male rhesus macaques have not been observed to fight for access to sexually receptive females, although they suffer more wounds during the mating season. An increased likelihood of attacks appears to coincide with male troop entry. Males who spend more time in consort and mate with more females tend to sire more offspring. Genetic analysis of paternity has pinpointed age and endurance rivalry, rather than agonistic competition, as key variables associated with variation in progeny production. Female rhesus macaques often copulate with multiple males during their ovulatory period, and tend to conceive on the first cycle of the mating season. Female reproductive success is more likely to be a function of offspring survivorship than the identity of particular male partners. The role of female choice as a direct mediator of male reproductive success is unresolved, but female mate selection seems to indirectly affect male reproductive success because female preference for mating with novel males seems to foster male dispersal. Evaluating whether mating preferences for particular male phenotypes affectsfemale reproductive success is a task for the future. A common denominator to the reproductive strategies of both female and male rhesus macaques is that feeding patterns affect body condition which influences reproductive output and regulates relative reproductive success.     

Variation in singing style use in the reed bunting Emberiza schoeniclus: influencing factors and possible functions

The two main functions of bird song are territory defence and mate attraction. Considerable progress has been made in understanding how species adjust the use of songs to serve these and other (presumed) functions of bird song, but the striking variety of singing behavior observable in wild birds remains enigmatic. Some species make do with simple songs and small repertoires, while others show large, complex repertoires and still others have evolved several distinct singing styles. In most species with distinct singing styles, however, the functions of singing styles are poorly understood. Two distinct singing styles (type I and II, respectively) have long been known in the reed bunting Emberiza schoeniclus, while a new third one has recently been reported to exist. We first quantitatively investigated the evidence for the existence of three singing styles. Then, we tested predictions of the mate attraction hypothesis, the mate guarding hypothesis and the territory defence hypothesis by examining the relations between singing style use with social and temporal factors. Cluster and discriminant analyses supported the existence of three (instead of two) singing styles, which could be differentiated based on four variables referring to song structure and complexity. Use of singing styles was related to male mating status (consistent with the mate attraction hypothesis), but not to female breeding stage (no support for the mate guarding hypothesis). Finally, use of singing styles differed in relation to time of day, with the dawn chorus of paired reed buntings consisting almost exclusively of songs of the recently discovered type III singing style and daytime singing primarily consisting of songs of long‐known type I (in unpaired males) or II singing styles (in paired males). Our findings suggest that one singing style (type I) primarily serves to attract a social mate, although an additional territorial function of this singing style cannot be dismissed. The function(s) of the other two singing styles, both only sung by paired males, are not related to attraction of a social mate or to the own female's fertility, but appear to be important in the context of territory defence and extra‐pair matings.     

Adaptive mating strategies and the problem of mate retention

"Adaptations" are evolved solutions to the problems posed by survival and reproduction. The evolutionary psychologists believe that as well as the physical adaptations so the adaptations in human mind evolved, called "strategies". The "mating strategies" are adaptive solutions to successful mating. The mating strategies, designed to preserve access to a mate by preventing encroachment of intrasexual rivals and by preventing a mate from defecting from the mateship for a prospective better partner, are called "mate guarding strategies". The previous research found that humans do use a wide variety of behavioural tactics of mate guarding, ranging from vigilance to violence. Our research group explores the type and the intensity of behavioural tactics of mate guarding used in several contexts. Presently, the link between the woman's fertility status across her menstrual cycle and the man's mate guarding is examined. Discussing the preliminary results, a more intensive man's mate guarding of his partner around the ovulation when her fertility peaks may be assumed. These outcomes could be explained as an adaptive prevention to shift in woman's preferences to increase her extra-pair sexual attempts and following to a possible genetic cuckoldry at that most fertile time.     

Insects and incest: Sib‐mating tolerance in natural populations of a parasitoid wasp

Sib‐mating avoidance is a pervasive behaviour that is expected to evolve in species subject to inbreeding depression. Although laboratory studies provide elegant demonstrations, small‐scaled bioassays minimize the costs of mate finding and choice, and thus may produce spurious findings. We therefore combined laboratory experiments with field observations to examine the existence of inbreeding avoidance using the parasitoid wasp Venturia canescens. In the laboratory, our approach consisted of mate‐choice experiments to assess kin discrimination in population cages with competitive interactions. A higher mating probability after sib rejections suggested that females could discriminate their sibs; however, in contrast to previous findings, sib‐mating avoidance was not observed. To compare our laboratory results to field data, we captured 241 individuals from two populations. Females laid eggs in the lab, and 226 daughters were obtained. All individuals were genotyped at 18 microsatellite loci, which allowed inference of the genotype of each female's mate and subsequently the relatedness within each mating pair. We found that the observed rate of sib‐mating did not differ from the probability that sibs encountered one another at random in the field, which is consistent with an absence of sib‐mating avoidance. In addition, we detected a weak but significant male‐biased dispersal, which could reduce encounters between sibs. We also found weak fitness costs associated with sib‐mating. As such, the sex‐biased dispersal that we found is probably sufficient to mitigate these costs. These results imply that kin discrimination has probably evolved for purposes other than mate choice, such as superparasitism avoidance.     

Social cues elicit sexual behavior in subordinate Damaraland mole-rats independent of gonadal status

Damaraland mole-rats (Fukomys damarensis) are among a small number of eusocial mammals. Eusociality is a social system where only a few individuals within a colony engage in direct reproduction, while remaining subordinate members are non-breeders and support reproductive efforts of breeding individuals. Inbreeding avoidance precludes mating between subordinate siblings and between offspring and parents. Interestingly, non-breeders readily attempt to mate with unrelated opposite-sex individuals. This is unusual since the non-breeding females do not attain puberty while in their natal colony. Based on this finding, the present study investigated the role of the gonads in the regulation of mating behaviors in this species and identified the mechanism of inbreeding avoidance. Gonadal-intact and gonadectomized non-breeders from different colonies were removed from their colonies and tested for the expression of sexual behavior. Results indicated that gonadal status had only minor effects on the expression of sexual behavior in either males or females. In a second experiment, sexual behaviors were absent between opposite-sex siblings so long as they had frequent contact with each other; however, following 5 weeks of separation, sexual behavior between these siblings was robustly expressed. Thus, Damaraland mole-rats avoid establishing mating relationships with familiar individuals but will readily mate with unfamiliar individuals of the opposite sex, with genetic relatedness apparently playing little role. The initiation of sexual behavior in Damaraland mole-rats does not require the presence of the gonads, but does require that the members of the pair have not been in contact with one another for at least several weeks.     

The relation among emergence date,days until first effective mating,fecundity and adult longevity in Isoperla aizuana and Sweltsa sp. (Plecoptera)

The relation between emergence date and the factors concerned in reproduction were studied in the stoneflies Isoperla aizuana (Perlodidae) and Sweltsa sp. (Chloroperlidae) in the laboratory. Individuals emerging earlier had larger adult size and greater adult longevity. Fecundity was also related to emergence date, adult size, and adult longevity. Furthermore, individuals emerging earlier had more days until first effective mating and tended to mate more effectively than later-emerging individuals. The maturity of the reproductive tissue may differ with emergence date. While most of the later-emerging individuals had a lower rate of effective mating, longer-lived and larger size adults mated more effectively in females of Sweltsa sp. The differences in mating character might affect the effectiveness of mating.