In humans, superior cognitive abilities and innovativeness are generally associated with affirmative (social, sexual) life outcomes (e.g., Plomin and Deary, 2015). However, the association between innovative problem-solving capabilities and their effects on mate choice, reproduction and fitness in non-human mammals is frequently neglected. Innovativeness facilitates survival in complex or changing environments, and allows individuals to explore and colonize novel habitats (Sol et al., 2005). Despite the obvious ecological and evolutionary benefits of being innovative (Laland and Reader, 1999; Nicolakakis et al., 2003; Reader and Laland, 2003), variation within a species, between the sexes, and across different species is only starting to be studied in more detail. For instance, behavioral studies revealed that primates and hyenas share similar socio-cognitive abilities. Elevated levels of innovativeness compared to other carnivores (Benson-Amram and Holekamp, 2012; Benson-Amram et al., 2016) have been observed in wild vervet monkeys (Cercopithecus aethiops) as well as in spotted hyenas (Crocuta crocuta). Aiming to determine whether innovativeness might be an adaptive trait in (female) spotted hyenas, Johnson-Ulrich et al. (2019) analyzed innovativeness in problem-solving tests in 29 female individuals and set these alongside long-term data on their fitness, reproduction and survival. They found innovative females to reproduce more cubs; however, their cubs showed a lower probability of survival compared to the fewer cubs of non-innovators. Hence, choosing a mate with superior cognitive abilities seems to pay off initially, but does not translate into an increased likelihood of passing on one’s genes to the next generation in the long run. Huebner et al. (2018) examined possible associations between body condition, survival rates, individual cognitive performance on repetitive attempts to solve a food extraction task (removing a sliding cover placed on small boxes to access a food reward), and spatial learning in a four-arm maze in wild gray mouse lemurs (Microcebus murinus). The cognitive ability to adopt a newly discovered technique to exploit novel food sources in times of scarcity quickly could provide them with significant fitness advantages. This pronounced ability should impress a female when observing and, finally, choosing a mate, as she could derive better nurturing of her offspring. However, neither the individuals’ cognitive performance in both tasks correlated with each other, nor did the performance correlate with the gray mouse lemurs’ survival rates (Huebner et al., 2018).

Sociality within a cohabitant community or population is also a relevant dimension in the context of cognition and mate choice. Williams et al. (2020) examined the direct and indirect effects of social position and individual behavioral traits on solving a novel puzzle box in social yellow-bellied marmots (Marmota flaviventer). Social relationships, the type of interaction and the individual role (i.e., recipient or initiator) significantly determined the way an individual interacted in cognitive tests. Interestingly, living a very social lifestyle resulted in lower reproductive success, increased hibernation mortality and, consequently, lower survival rates in female but not in male yellow-bellied marmots. Especially young females and their offspring greatly benefited from larger social groups. Again, this effect was not observed in males regardless of age (Montero et al., 2020). Conversely, the strength of affiliation was negatively associated with female annual reproductive success (Wey and Blumstein, 2012). These findings clearly indicate that social behavior, social and/or sex roles, and cognitive abilities not only play an important role during mate choice and reproduction, but also seem to translate in the probability of the own and/or the offspring’s survival in a positive or negative way. Male meadow voles defend large home territories against conspecific rivals and their reproductive success is closely linked to finding females to mate with. Indeed, the courting males’ spatial learning ability is considerably more pronounced compared to their conspecific females (Gaulin and FitzGerald, 1986, 1989; Galea et al., 1996). As is the case with many rodents, they typically leave their scent on prominent landmarks or along trails to ensure that they are perceived by conspecifics of both sexes. The scent marks provide various social information, such as sex, reproductive state, health condition, or social rank. The odor information targets different recipients (e.g., receptive females, competitors or heterospecifics), who in turn classify its relevance and value according to its phenotype, genotype, and intentions. Hence, depending on which animal encounters the scent mark, it has to compare the social odor information with memorized details and make various decisions relating to, for instance, mate choice, same-sex competition, social olfactory communication, or sperm distribution/competition. In addition to the availability of mates and resources, the own fitness, age, sex, and social position play a key role to ensure survival and to improve the own fitness. As a result, a complex, associative social memory develops to identify scent marks as being, e.g., from males or females, as known or unknown, as sexually immature or receptive. However, as scent marks of different animals may overlap, complex supporting cognitive capabilities are required to form appropriate associations and adapt behavior accordingly (Ferkin, 2011, 2018).

Many studies on mate choice in birds focus on physical traits, but aspects of individual personality and social alliances are also receiving increasing attention. In particular, in long-lived avian species, social alliances that form at pre-mature life stages (i.e., prosocial behavior) apparently lead to long-term social bonds (parenthood, long-term cooperative pair and/or group behavior) at a sexually mature age (Kaplan, 2020). Examples of prosocial bird species, who are known for their exceptional cognitive abilities, include jackdaws (Corvus monedula) (De Kort et al., 2006; von Bayern et al., 2007; Schwab et al., 2012), Eurasian jays (Garrulus glandarius) (Ostojić et al., 2013, 2014), rooks (Corvus frugilegus) (Scheid et al., 2008), common ravens (C. corax) (Di Lascio et al., 2013; Massen et al., 2015), or even African gray parrots (Psittacus erithacus) (Péron et al., 2013). In this context, sociality including its cognitive and affective dimensions, and mate choice might play a key role in birds in terms of a “pre-sexual attachment to a potential mating partner” (Kaplan, 2020).

In a wide range of avian species, strong relationships were discovered between the length of parental brood care and brain size, raising suggestions of related enhanced cognitive capabilities. These suggestions were supported by observations, for instance, in several corvids, bowerbirds, albatrosses, and cockatoos, which revealed prolonged parental guidance just until the first own brood to be an essential component in the acquisition of social and cognitive skills (Kaplan, 2020). To give an example, the sexual display of male song is generally considered a sex-specific social behavior that is learned prior to sexual maturity and presumably requires elevated cognitive skills in both sexes (Boogert et al., 2011b; Peters et al., 2014; Anderson et al., 2017). Most bird song research has been performed assuming that songbirds have evolved complex song repertoires due to the pressure of sexual selection on males that arises from both competition between males and female choice (Beecher and Brenowitz, 2005; Byers and Kroodsma, 2009). Interestingly, learned aspects of song have been found to alter female mating preferences in various songbird species (DuBois et al., 2018), although females usually do not sing themselves. It is important to note, however, that females of more than two-thirds of all songbird families also sing in contexts such as tropical dispersal, territoriality, convergent sex roles, and sexual dichromatism. In many species, however, females have lost song secondarily (compare Odom et al., 2014 for review).

Several studies on the relationship between a male’s vocal repertoire and various cognitive processes try to determine whether the male’s song may provide conspecific females with information on his cognitive abilities (Boogert et al., 2011b; Sewall et al., 2013; Anderson et al., 2017). So, sex roles appear to be clearly assigned in many songbird species: while males sing as part of their courtship display, females listen to and evaluate the quality of the males’ song. Although the neuronal prerequisites that guide the complex process of singing and song composition in male and female songbirds are well understood (Nowicki et al., 2002; Gobes and Bolhuis, 2007; Mooney, 2009; Jin, 2013; Sewall et al., 2013; Geberzahn and Aubin, 2014; Odom et al., 2014), there is still a lack of understanding of the relationship between song learning and other cognitive processes (Anderson et al., 2017) in the context of mate choice. Female songbirds prefer males presenting a larger vocal repertoire (Searcy, 1984; Lampe and Saetre, 1995) and song is deemed an honest signal of male quality and fitness measures. In male song sparrows (Melospiza melodia), song repertoire size correlates positively with an array of fitness traits comprising territory ownership, heterozygosity, immune system quality, longevity, and lifetime reproductive success (Reid et al., 2005; Boogert et al., 2011a). In a 20-year-long-term study, Reid et al. (2005) analyzed data from free-living male song sparrows (M. melodia) in terms of song repertoire size and the number of independent and recruited offspring and grandoffspring. The larger the song repertoire was, the longer-lived the males were and the greater was their reproductive success extending into the next and even the succeeding generation. Wild female song sparrows (M. melodia) prefer males with a rich vocal repertoire, which also correlates with various fitness measures (e.g., song repertoire size and different motor, color association, reversal learning or detour-reaching tasks tested in captivity, Boogert et al., 2011a,b; DuBois et al., 2018). Moreover, song complexity as a sexual signal has been linked to male zebra finch performance in a novel foraging task (Taeniopygia guttata castanotis, Boogert et al., 2008). Conversely, Sewall et al. (2013) challenged song sparrow males (M. melodia) in a spatial memory task and discovered an inverse relationship between spatial memory performance and male vocal repertoire.

Associations between song repertoire size and cognitive performance were examined in wild song sparrows (M. melodia). Initially, males’ song repertoires were recorded in the field. Subsequently, these males were tested in motor, color association and reversal learning, and detour-reaching tasks (Boogert et al., 2011a,b). The individuals’ color association performance was positively correlated with their performance in the subsequent reversal task. Interestingly, their performance did not correlate with the other learning tasks they were challenged with. Nevertheless, males having a wider song repertoire were able to solve difficult tasks in a shorter period of time, but performed poorly in the reversal task compared to males having a more limited song repertoire (Boogert et al., 2011a,b). Yet, results remain inconclusive as no correlations were observed in laboratory-raised song sparrows following the same experimental agenda (Anderson et al., 2017). In a recent study, a group of 49 swamp sparrows (Melospiza giorgiana) was examined for their song quality (i.e., repertoire size, vocal performance, song learning; DuBois et al., 2018). Subsequently, song quality was compared to the performance in five different cognitive tests, comprising a novel foraging task, a color association and a reversal task, a spatial learning task, and a detour-reaching task. Unexpectedly in the context of the previous study by Boogert et al. (2011b), none of the song parameters were considered indicative of any cognitive performance level. Hence, these findings contradict the hypothesis on song properties indicating overall cognitive abilities in swamp sparrows (DuBois et al., 2018). Likewise, no associations between song repertoire and cognitive performance (detour reaching, spatial memory) were obtained when testing wild North Island robins (Petroica longipes), which are a foraging species, admittedly with a quite different ecology than sparrows (MacKinlay and Shaw, 2019). In summary, there remains controversy about the phenomenon of bird song and its implications for cognitive mate choice (compare Searcy and Nowicki, 2019 for review).

However, several studies on different bird species attempted to investigate associations between cognition and mate choice from different perspectives. In food caching New Zealand robins (P. longipes), males’ memory performance in a spatial task during winter severely influenced their subsequent breeding success. Individuals with higher performance levels produced more fledglings and, subsequently, more independent offspring per nesting attempt. Males with superior memory performance spent more time in flight while foraging and provisioning, and, additionally, provided their chicks with an increased share of large prey items. These effects were absent in female robins (Shaw et al., 2019). Male bowerbirds spend a considerable amount of time building their bowers to attract females and convince them to mate. Several studies revealed that the male satin bowerbirds’ mating success was positively associated with their problem−solving performance and aggregate measures of their cognitive ability (Keagy et al., 2009, 2011). The males were challenged with six different cognitively challenging tasks, including two problem-solving tasks, one mimetic repertoire task and three bower-rebuilding tasks. Although no correlations between the males’ performances in different tasks were observed, females chose the overall well-performing males, thereby apparently considering information about several behavioral display traits (Keagy et al., 2012). However, Isden et al. (2013) reported conflicting observations by finding no relationship between performance on cognitive and problem-solving tasks and mating success in male spotted bowerbirds.

Two studies, one using zebra finches (T. guttata castanotis; Chantal et al., 2016) and the other using budgerigars (Melopsittacus undulatus; Chen et al., 2019) explored whether females would modify their mating preference after having observed the cognitive performance of males in a problem-solving task:

Initially, zebra finch females were challenged with a set of two males to assess their spontaneous preference for one or another (Chantal et al., 2016). Then, both zebra finch males (i.e., the preferred and the unpreferred one) were trained to open a tube by removing the lid to access a food reward (Chantal et al., 2016). In order to manipulate their success, one male (the previously unpreferred male, now assigned to be the ‘solver’) was challenged with a tube the lid of which was pressed only halfway and which could be easily opened. The other male (the previously preferred male, now assigned to be the ‘non-solver’) was challenged with a tube the lid of which was fully pressed and, thus, was impossible to open. Subsequently, females were allowed to observe both males being challenged with the tube-opening task. In contrast to the first preference test, females preferred the solvers, i.e., the previously unpreferred males in the final second preference test. To determine (a) whether females were able to discriminate between both males and (b) whether the males’ problem-solving abilities had in fact triggered the shift in female preference, all birds took part in a color association task. Females were well able to discriminate visually between the presented males, and their preference was found to be independent of the males’ learning rate in this task. Considering the results of both tasks in a shared context, zebra finch females were found to significantly prefer the most skillful (i.e., the initially unpreferred) male in both tasks. As males differed in their feeding rates in both treatments, females appeared to use the males’ foraging efficiency as an important criterion when choosing a mate (Chantal et al., 2016).

The other study (Chen et al., 2019) followed a similar experimental design, in which budgerigar females were challenged initially with a set of two males to assess their spontaneous preference for one or another as well. Then, non-preferred male budgerigars were trained to open transparent boxes containing seeds. Meanwhile, the preferred males and females were exposed to already-opened containers, so they could not attempt to solve the following foraging task. Subsequently, each female was allowed to observe the trained (but initially unpreferred) males repetitively opening the boxes, while the untrained (but initially preferred) males failed. In consecutive second preference test trials, females changed their social preferences in favor of the successful, formerly unpreferred males. Control tests suggested that the females’ preference shift did not only reflect the observation of trained males feeding on seeds, i.e., the males’ ability to provide food. Furthermore, females showed no preference for other females trained to open the seed boxes, indicating that the main finding related to an intersexual context (Chen et al., 2019).

However, even with these two carefully designed studies, which have yielded impressive results, we cannot be entirely convinced that cognition was the main factor in the females’ choice. First, neither zebra finch nor budgerigar females were allowed to attempt the problem-solving tasks (i.e., zebra finches opening tube lids or budgerigars opening boxes) themselves. Yet, in order to be able to evaluate and, subsequently, rank the males’ individual abilities in solving a particular task, the judge herself needs to be aware of the complexity of the task she is now meant to assess. It is therefore difficult to predict the extent to which the zebra finch or budgerigar females were able to assess the cognitive aptitudes of the males performing the test. Second, neither zebra finch nor budgerigar females were allowed to observe the males while learning and, thus, examine differences in the males’ learning processes. Hence, females exclusively witnessed the output of the preceding training, which was attended only by a selection of the males. Third, the zebra finch and the budgerigar males’ success in problem solving was manipulated in both studies, either by closing the tubes at varying degrees of tightness (Chantal et al., 2016) or by training only the unpreferred males (Chen et al., 2019). Instead of assessing cognitive problem-solving abilities, the observing females may have interpreted the differences in males’ ability to access the containers as differences in the males’ physical strength (Striedter and Burley, 2019). Indeed, the training itself could have had an impact on the males’ behavior. Different degrees of training might have also been a reflection of different levels of male self-confidence or audacity in approaching the task in the female’s presence, which, potentially, could have influenced her choice. For instance, the trained (initially unpreferred) males may have acted more keenly when handling the tubes or containers since they were already acquainted with the experimental setting, while the inexperienced (but initially preferred) males were not. Hence, this raises the question of the extent to which personality traits such as boldness, shyness, retentiveness, or self-confidence, i.e., an individual’s cognitive style play an important role in (a) approaching cognitive tasks, and in (b) assessing cognitive abilities by potential mates. Camacho-Alpízar et al. (2020) added another perspective by questioning whether successful problem-solving can be linked to cognitive abilities at all, as “non-cognitive factors (e.g., persistence) are often correlated with problem-solving success”.

Beyond mammals and birds, an increasing number of studies addresses the role of cognition in mate choice of various fish species. Relative to all vertebrate taxa, fish do not only represent the greatest species diversity, but also inhabit the most diverse physical and social environments. They are characterized by the greatest variation in brain anatomy of all vertebrates. This gives them the neuronal basis for different levels of behavioral plasticity in response to their environment. In turn, this suggests, hypothetically, an equivalently wide variety of cognitive traits relating to social interactivity and mate choice. Many fish species can flexibly adapt their physiology and behavior to cope better with challenging environmental conditions. In fact, a major component of this flexibility is supported and influenced by both cognition and neuronal plasticity (Ebbesson and Braithwaite, 2012; Herczeg et al., 2019). Novel foraging information propagates considerably faster between female guppies than between males, possibly because the reproductive success of female guppies is inherently more strongly linked to resource availability than it is the case for male guppies (Reader and Laland, 2000). Male guppies (P. reticulata) were trained to solve two different mazes to obtain a food reward (Shohet and Watt, 2009). Subsequently, female guppies were allowed to repeatedly observe several different trained males orienting within the maze. Consecutive mating preference tests as well as the time it took a male to learn both mazes were used to determine a possible association between the females’ preferences and the males’ learning ability. Indeed, the observing females preferred the faster-learning males, who they judged to be more attractive than the slow learners in subsequent mating preference tests. Furthermore, the females’ preference was not related to the males’ body size or coloring, although males of a stronger orange color solved the tasks faster than their less colorful peers. Similar to the bird studies (Chantal et al., 2016; Chen et al., 2019), guppy females were unfortunately not allowed to observe the males while learning to pass through the mazes, nor were the females themselves challenged with any maze in order to be able to judge the level of difficulty and/or the males’ performance. Consequently, we cannot fully reject the objection that females may have taken into account any other, unmeasured traits such as the males’ display rates (Matthews et al., 1997; Kodric-Brown and Nicoletto, 2001) or the males’ general mobility (Van Oosterhout et al., 2003) to base their preference on. Results were supported by findings in sailfin tetras (Crenuchus spilurus) using a comparable test paradigm. At the same time, the highly ornamented males were considerably more neophobic than their less ornamented rivals, presumably because they experience greater predation pressure while also having a higher predicted fitness payoff (da Silva Pinto et al., 2021). Accordingly, sexual selection by means of female preference seems to result in greater cognitive abilities of smart, beautiful males, whereby cognition is becoming a vital part of their attractiveness to females.

A study on male threespine sticklebacks (Gasterosteus aculeatus) examined a very different aspect of cognition, namely inhibitory control, which may possibly be related to male sexual signals (Minter et al., 2017). Inhibitory control describes a cognitive process, which enables an individual to inhibit its natural, habitual, or dominant behavioral response to certain stimuli for adopting a more appropriate behavior to meet its intended goals (Hauser, 1999; Boogert et al., 2011b; Bray et al., 2014; Rystrom et al., 2019). In threespine sticklebacks, males provide all parental brood care, but at the same time, they need to avoid eating their own fry that closely resemble their prey. Hence, males with better inhibitory control would be more successful in rearing their offspring, resulting in higher fitness levels. Initially, male sticklebacks were challenged with a detour-reaching task. Subsequently, the males were assessed for their sexual signals (coloration, nest area and courtship vigor) to determine whether this visual information would reveal the males’ cognitive abilities, which proved not to be the case. Females preferred to mate with males that showed better initial inhibitory control, suggesting that females possibly consider this male trait as a crucial trait for mate choice (Minter et al., 2017). Keagy et al. (2019) reported similar results, revealing that neophobia differences between both sexes allowed male threespine sticklebacks to consistently outperform females in a detour task. However, unlike female sticklebacks, who preferred cognitively superior males (Minter et al., 2017), male sticklebacks did not express this preference when choosing females (Keagy et al., 2019). Hence, we may derive two possible lessons: either males merely disregarded the females’ cognitive performance in the present task when courting a female to mate with or the chosen detour task did not adequately reflect their preference for aspirational female cognitive skills.

In answering the first key question ‘Do cognitive skills guide an individual’s mate choice and, ultimately, does learning change an individual’s decisions?’, we can conclude that (a) sexes differ in their cognitive abilities depending on the given challenge, presumably because of the different roles they play within their social community. This suggests that the cognitive processes governing their mate choice decisions will also differ. Moreover, we can deduce that (b) cognitive abilities indeed have a considerable influence on individual mate choice decisions in species across different taxa, and (c) the males’ displays of learned behavioral patterns alter the females’ mate choice decisions. We can draw these conclusions for three large vertebrate taxa – i.e., mammals, birds and fish. Further research should aim to expand our knowledge to amphibians and reptiles, which have been less extensively examined in this field so far.