Aims and Objectives
This Special Column aims at complementing our knowledge and deepening our understanding
of the complex processes involved in learning and neurobiological mechanisms in the
context of sexual selection.
So far, there are a number of studies dealing with specific aspects in neurobiology
OR sexual selection, however, there is no comprehensive account of studies linking
neurobiological aspects with mate choice to this date. For instance, various studies
investigate sex differences in a wide range of cognitive and behavioral processes
in a variety of vertebrate and invertebrate groups. But investigations of sex differences
in (social) learning and, for example, memory AND the underlying neurobiological substrates
in the context of sexual selection and their importance in mate choice behavior have
been largely neglected. Thus, studies combining learning and cognitive abilities with
neurobiological substrates in the context of mate choice are still rare. Critical
questions that remain to be answered include why and how does learning and cognition
influence mate choice? How do environmental conditions affect the evolution of the
underlying neurobiological substrates? Which neural circuits are shared or distinct
between sexes within species and/or between species of the same and/or different taxonomic
groups?
Sexual Selection
In the 1970s and 1980s, sexual selection became a popular focus of research in evolutionary
biology and various related aspects are still being investigated today. Even though
many of the fundamental processes, mechanisms, and phenomena of sexual selection (Parker
and Pizzari 2015; Hill 2015; Rosenthal 2017) remain the subject of intense discussions,
a number of basic questions continue being unaddressed; despite the fact that these
questions date back to Darwin’s time (1871). Darwin (1871) described 2 “modes” of
sexual selection: intrasexual selection acts via competition “between the individuals
of the same sex, generally the males, in order to drive away or kill their rivals,
the females remaining passive; whilst in the other, the struggle is likewise between
the individuals of the same sex, in order to excite or charm those of the opposite
sex, generally the females, which no longer remain passive, but select the more agreeable
partners” which is intersexual selection. These forces (“male competition”, “female
choice”) mirror striving for the best possible mating partner. However, both sexes
show both intrasex competition and intersex mate choice — although these are frequently
weighted differently in sexes and/or species. However, competition and strategic mate
choice are only 2, albeit behaviorally conspicuous and, therefore, well studied mechanisms
of sexual selection. In addition, less obvious strategies such as sperm competition
or manipulative and exploitative behavior driven by sexual selection (e.g., deception,
infanticide, and sexual violence) exist. Sexual competition results in winners and
losers. If individual males are unlikely to succeed in the competition for sexual
partners, but are most likely among the losers, it is often more advantageous for
them to evade the unfavorable form of competition and instead try to achieve their
fitness goals through “alternative tactics”. These may include, for instance, strategies
taking into account physical sex-specific dimorphism, the “social rank” of an individual,
enhanced cognitive capabilities such as learning or remembering of food sources, using
public information about the social and ecological environment, or a higher degree
of behavioral flexibility. However, we are only beginning to understand the way in
which sexual selection responds, interacts and, in turn, is influenced by other processes
and phenomena.
Mate Choice and Cognitive Abilities
Mate choice occurs within a complex framework of an animal’s social interactions that
are markedly affected by factors such as envi-ronmental conditions, cognitive abilities,
dominance hierarchies, family bonds, age, or sex of an interacting individual. Moreover,
attention, motivational, sensory, and perceptual mechanisms (all of which are known
to exhibit substantial differences between sexes and species) that allow animals to
survive, cooperate, and reproduce depend on the corresponding morphological and/or
neuronal prerequisites innate to every individual. Mate choice has favored the development
of a wide diversity of sexual signals to attract the choosy sex (Bateson 1983). For
instance, given the great variety of beautiful male ornaments, it is difficult to
deny the females any preference, as even a slight preference would allow sexual selection
(Jones and Ratterman 2009). Hence, Darwin (1871) observed that “when we see many males
pursuing the same female, we can hardly believe that the pairing is left to blind
chance – that the female exerts no choice, and is not influenced by the gorgeous colours
or other ornaments with which the male alone is decorated”. But why should female
preferences exist at all? Females receive both direct and indirect fitness benefits
for their offspring by exploiting these signals to determine the best and most suitable
partner (Kokko et al. 2003). However, there is often a wide, highly individual variation
in the choosy sex’ preferences, which is likely to affect the strength and di-rection
of sexual selection on particular characteristics within a population (Brooks and
Endler 2001). In the past, numerous studies have focused on determining behavioral
and physical traits indicative of the quality of preferred partners (Andersson 1994;
Schuett et al. 2010). More recently, research has shifted one focus toward the examination
of the congenital cognitive or behavioral characteristics of choosing individuals
as well as on those that are chosen, and how these initiate and/or influence mate
choice of the choosy sex. For instance, it has recently been shown that problem-solving
tasks (Chen et al. 2019), sensory characteristics (Ronald et al. 2018) as well as
brain size (Corral-López et al. 2017) in females significantly affect mate choice
and the ability to accurately assess the sexual signals of potential mating partners.
In this context, individual cognitive differences may contribute to better explaining
the varying preferences for one or another sexually selected trait, which, for instance,
may be common within a particular population.
Recently, associations between an individual’s mating success and cognitive skills
(Shohet and Watt 2009; Keagy et al. 2009, 2011; Minter et al. 2017) and between its
cognitive skills and sexual characteristics (Karino et al. 2007; Boogert et al. 2008,
2011; Mateos-Gonzalez et al. 2011; Keagy et al. 2012; Fabre et al. 2014) have indicated
that sexual selection may possibly affect cognitive abilities (Andersson and Simmons
2006; Boogert et al. 2011; Sewall et al. 2013; Isden et al. 2013). Cognition is described
in terms of the way individuals acquire, store, and use information (Shettleworth
2010). For instance, this information can be applied to decisions on potential mating
partners and, thereby, possibly result in mate choice via learning. In this context,
mate choice involves personal experience with others (i.e., private or personal information)
or observing conspecifics (i.e., public information) and continues throughout an individual’s
entire life (reviewed in Hebets and Sullivan-Beckers 2019). Moreover, environmental
— including social—influences on mating decisions have long been recognized (Jennions
and Petrie 1997; Irwin and Price 1999). Throughout their lives, animals gather and
process environmental information, that is, these individuals learn (cf. definitions
of “learning” in Barron et al. 2015). Accordingly, their learning and decision-making
processes can have a social component and may change to increase their chances of
finding a high-quality partner. An individual’s “cognitive style” comprises many aspects
of cognition such as an individual’s cognitive flexibility, decisiveness, or gathering
of new information (Sih and Del Giudice 2012), and individuals within populations
were observed to exhibit homogeneous differences in cognitive style (Matzel et al.
2003, 2017; Guillette et al. 2015; Boogert et al. 2018).
Sex Differences in Cognitive Abilities in the Context of Mate Choice
Variations in the way cognition is associated with different sex roles potentially
lead to differences in selection on cognition and possibly trigger sex differences
related to cognitive abilities (Galea et al. 1996; Jacobs 1996; Lindenfors et al.
2007). In various species across all taxa, this “cognitive-sexual dimorphism” often
reflects the observed differences in sex roles within a mating system. Male cognition
has been identified as an important potential protagonist in sexual selection. Various
studies have determined positive associations of male sexual signals with cognitive
performance and/or significantly increased preferences of females for males that perform
better cognitively. For instance, meadow vole males Microtus ochrogaster, M. pennsylvanicus
dominate large home ranges and their reproductive success is strongly correlated with
finding and convincing females to mate. To meet these challenges, meadow vole males
developed an improved spatial learning ability compared with their conspecific females
(Gaulin and Fitzgerald 1986, 1989; Galea et al. 1996). Likewise, male guppies Poecilia
reticulata outperformed females in learning a complex spatial task (Lucon-Xiccato
and Bisazza 2017) and made decisions faster (though not more correct) than females
in visual color discrimination learning (Lucon-Xiccato and Bisazza 2016). Conversely,
female guppies were observed to outperform males in a spatial orientation task to
rejoin a group of conspecifics and in a numerical task requiring them to discriminate
between 5 and 10 dots to obtain a food reward (Petrazzini et al. 2017). Another study
examined western mosquitofish Gambusia affinis regarding the association between activity,
exploration, anxiety, and sociability with the individual’s associative learning performance
in numerical discrimination experiments (Etheredge et al. 2018). The authors concluded
that sexes differ in their cognitive-behavioral responses that could possibly be attributed
to different sexual selection pressures, despite the convergence of their learning
performance (Etheredge et al. 2018).
Cognition and Behavioral Flexibility
While many mating preferences have a genetic basis, the question remains as to whether
and how learning and/or experience can alter an individual’s mate choice decisions.
The ability to learn from experience offers a certain degree of flexibility which
is crucial to living in a variable, constantly changing environment (Dodson 1988).
In this context, “behavioral flexibility” denotes the ability to better adapt the
own behavior to altered environmental conditions or unpredictable resources (Bond
et al. 2007). It requires individuals to rapidly shift from a no longer viable strategy
to a new one to obtain new associations as environmental demands change (Rayburn-Reeves
et al. 2017a,b). Therefore, assessing an individual’s behavioral flexibility allows
to indirectly examine its level of “cognitive flexibility”. Cognitive flexibility
has been defined as the ability to channelize attention between different tasks, for
instance, in response to an alteration of rules or demands (Scott 1962). Accordingly,
it is the aptitude to adapt the own rational to new situations and/or to overcome
the habitual thinking and decision-making processes (Deak 2003; Moore and Malinowski
2009; Rayburn-Reeves et al. 2017a,b).
In several mammalian, avian and fish species, females were observed to show a higher
performance than males in tasks requiring cognitive flexibility such as the discrimination
reversal learning. For instance, female guppies appeared to be more innovative and
interested in problem solving when given a novel foraging task involving spatial exploration
(Laland and Reader 1999). Likewise, females solved learning flexibility tasks faster
compared with their male conspecifics. In these studies, individuals were challenged
either with a detour reaching task to join a group of conspecifics (Lucon-Xiccato
and Bisazza 2017) or with a series of color discrimination reversal learning tasks
(Lucon-Xiccato and Bisazza 2014).
To widen our understanding of the ways in which learning, other neurobiological aspects,
and mate choice interact, coincide or differ between males and females within or between
species, the topical collection of this Special Issue comprises a number of exciting
contributions: Keagy et al. (2019) observed cognitive sex differences and their relationship
to male mate choice. To do so, they repeatedly presented male and female three-spined
sticklebacks Gasterosteus aculeatus with a detour task to assess initial inhibitory
control and improvement over time, and examined, whether male mate choice was associated
with female inhibitory control. Since males consistently outperformed females, there
seemed to be suggestive evidence that males learned the task better than their conspecific
females, although sex-specific differences in neophobia played an important role as
well. Rystrom et al. (2019) have examined the flip side of the same coin. They challenged
female three-spined sticklebacks with a dichotomous mate choice task using computer-animated
males differing in breeding coloration. They examined their results with regard to
the females’ spatial learning and reversal learning ability and possible correlations
between an individual’s spatial learning ability and its mate assessment. Females
spending more time to evaluate potential partners in a dichotomous mate choice task
made fewer errors during both the initial and reverse spatial learning task. However,
these females made more consecutive errors at the very beginning of the reversal phase,
indicating that they were not quickly adapting to environmental changes, but quickly
forming strict routines during the learning tasks.
Plath et al. (2019) have also focused on mate assessment to which they added the exciting
aspect of the attendances or absences of predators. They assigned wild-caught (predator-experienced)
and laboratory-reared (predator-naïve) Western mosquitofish G. affinis to 2 mate choice
tests, during one of which different animated pre-dators were present. They aimed
to investigate whether (innate) mating preferences would change under immediate predation
threat and whether potential predator-induced changes in mating preferences would
differ between sexes or depend on the choosing individual’s personality and/or body
size. Wild-caught fish altered their mate choice decisions most when exposed to co-occurring
predators whereas laboratory-reared individuals responded most to coevolved predators,
suggesting that both innate mechanisms and learning effects were involved. The effects
were stronger in bolder individuals, likely because those phenotypes face an overall
increased predation risk.
Within the scope of this Special Issue, sex-specific differences, visual discrimination
ability, and aspects of spatial orientation, although in different contexts have been
studied in túngara frogs and 3 poeciliid species. Ventura et al. (2019) tested male
and female túngara frogs for their place learning capabilities by using a 2-arm maze
featuring 2 differently marked doors (red, yellow, or achromatic cues), one of which
was rewarded with return to the home cage. They examined whether the type of door
marking (chromatic or achromatic) had a sex-specific effect on the individuals’ place
learning behavior. Frogs rewarded to choose the yellow door showed an increase in
correct choices and an increased preference for the yellow door in the course of training.
However, authors found no evidence for a sex difference in learning. Fuss and Witte
(2019) performed one of the first comparative studies dealing with behavioral flexibility
in the context of (cognitive) sex-specific differences in 3 related poeciliid species
(P. latipinna, P. mexicana, and P. reticulata). They assessed male and female individuals
for their ability to exploit previously gained knowledge using a simple color discrimination
paradigm (red, yellow, or green cues) and, subsequently, for their behavioral flexibility
in a series of reversal tasks. While no sex differences were observed in sailfin mollies,
male Atlantic mollies learned to solve the initial color discrimination task significantly
faster than their conspecific females. Surprisingly and contrasting our expectations
of a reflection of the results of a previous study on guppies (Lucon-Xiccato and Bisazza
2014), only females solved the initial task in our study, whereas males failed to
learn any of the tasks they were assigned to. Regarding the expected sex differences
in accuracy and behavioral flexibility during serial reversal learning, different
results for the 3 species under investigation were observed. Compared with previous
studies or other vertebrate taxa, the hitherto apparently universal pattern (i.e.,
females showing higher behavioral flexibility) seemed to be inverted in the 2 examined
molly species.
Sexual Selection and Neurobiological Substrates
Mate choice may involve any sensory modality (Halfwerk et al. 2019). Choosers often
attend to a courter’s traits by exploiting every modality they possess. However, prior
to a chooser expressing a preference for any particular aspect of a courter’s phenotype,
the chooser (i.e., the recipient) has to be capable of recognizing it (Levine 2000);
anything outside a chooser’s range of sensitivity is imperceptible to it, for example,
invisible, inaudible, or odorless (Rosenthal 2017). A stronger sensory stimulation
often translates into a stronger preference of a certain trait. In short, sensory
biology is of major importance to mate choice and to its evolutionary effects.
Vocalization plays an outstanding role in mate recognition and selection in a number
of taxa, especially, but not limited to, orthopterans, frogs, birds, and certain fish
species. The ability to unambiguously identify a conspecific by its vocalizations
alone, the so-called “individual voice recognition”, allows a fast, turning communication
in a crowd (e.g., Bee and Micheyl 2008). For instance, in a social context, such as
a cocktail party, it might be of vital impor-tance to recognize the voice of the spouse.
Individual voice recognition is widely spread amongst animals of various taxonomic
groups — especially, but not limited to orthopterans (e.g., Greenfield 2002), frogs
(e.g., Ryan 2001; Gerhardt and Huber 2002), birds (e.g., Keen et al. 2016; D’Amelio
et al. 2017), and some fish species (e.g., Amorim et al. 2015). Many mammalian and
bird species are even capable of vocally recognizing their partners, relatives or
group members (e.g., Lambrechts and Dhondt 1995; Frommolt et al. 2003; Insley et al.
2003; Sharp et al. 2005; Deecke 2006; Börner et al. 2016; Stoeger and Baotic 2017).
It is known, however, that several species generate a large number of different acoustic
signals that allow individuals to flexibly convey information in different contexts
with a large vocal repertoire (e.g., Bradbury and Vehrenkamp 2011). The acoustic information
presented in a sound signal needs to be decoded and processed by the recipients, which
sometimes can be a complex cognitive task (Zatorre and Schönwiesner 2011). To understand
the communication processes of a particular species, the (sexually dimorphic) characteristics
of the entire vocal repertoire, the morphological structures that generate or perceive
the sounds, as well as the recognition thresholds and the underlying neural substrates
evaluating the sensation need to be taken into account. For instance, the effects
of both natural and sexual selection can be traced back by observing (sex-specific)
acoustic communication in many anuran species. Within the scope of this Special Issue,
Taylor et al. (2019) aimed to investigate the threshold for signal salience of female
túngara frogs detecting male acoustic sexual displays. To do so, they compared differences
among behavioral signal recognition thresholds, midbrain multiunit electrophysiological
thresholds, and neural auditory brainstem thresholds of female túngara frogs in response
to simple tones and complex male advertisement calls. They revealed substantial differences
among signal recognition thresholds, electrophysiological thresholds, and auditory
brainstem thresholds. Fittingly, McClelland et al. (2019) focused on 2 main aspects
of the laryngeal and ear structures of cricket frogs Acris crepitans — the potentially
sexually dimorphic anatomical characteristics and the differences between populations
living in different habitats — in the context of allometric effects of body size.
Both sexes showed size differences in the larynx related to selection for larger body
size in dry, open habitats. However, the observed selection on males for larger larynx
size related to the production of lower frequency calls in those habitats did not
result in correlated changes in the female larynx.
Future Perspectives
The topical collection of this Special Issue opens new exciting perspectives on the
wide field of sexual selection and mate choice both in the context of sex-specific
cognitive abilities and flexible behavioral adaptations, and in the context of sex-specific
sensory–neurobiological characteristics. The various contributions can only scratch
the surface of the diversity of ways in which learning, morphology, and neuronal activity
can interact with mate choice and sexual selection. Hence, various aspects are brought
together allowing the drawing of well-deserved attention to this key issue of behavioral
and evolutionary biology.
With this Special Issue, we provide further evidence to Darwin’s hypothesis that mate
choice has an intriguing influence on the evolution of cognitive abilities in nonhuman
individuals. Unquestionably, it is and will continue to be fascinating to unravel
how superior cognition offers an evolutionary advantage, especially in terms of potential
benefits for reproductive fitness. In mammals and birds (González-Lagos et al. 2010;
Minias and Podlaszczuk 2017), those comparatively larger-brained individuals alleged
to have superior cognitive abilities, were observed to be more long-lived compared
with their smaller-brained conspecifics. For fish, a bigger brain will also come at
a price: larger-brained individuals were observed to be smarter, but had about one-fifth
less offspring than those with smaller brains (Kotrschal et al. 2013). On the contrary,
they might still be able to reproduce better (and increase their reproductive success)
because cognitive abilities contribute beneficially to survivorship in terms of foraging,
mate choice, or escape from predators. Although a considerable body of studies has
provided an impressive array of indirect evidence that cognition and attractiveness
interrelate closely, the ultimate proof for the choosing sex judging cognitive abilities
in potential mates just as outwardly visible physical traits is still lacking. In
a thoroughly planned and well-performed study on budgerigars, Chen et al. (2019) attempted
to bridge the gap between mate choice and cognitive traits, a link urgently needed
and often neglected in the fields of cognition and sexual selection. In this study,
female budgerigars altered their preference for males after observing these males’
ability to open 2 different so-called “problem boxes” to get access to food. This
shift did not occur in control experiments, neither when focal females observed females
solving the same task, nor when focal females observed males having free access to
food. However, when interpreting these results, cognition cannot serve as the only
explanation. Since females were not given the opportunity to explore the foraging
task themselves to be able to judge the males’ cognitive performance. They could also
have attributed a male’s problem-solving ability to its physical strength or subtle
behavioral differences elicited by the extensive training paradigm (Keagy et al. 2019;
Striedter and Burley 2019). Thus, in the context of this study and the studies in
this Special Issue, it will remain a fascinating challenge to explore why and how
learning and cognition do indeed influence mate choice and the dynamic processes in
sexual selection and how (social) environmental conditions may affect the underlying
neural substrates.