Machteld N. Verzijden

The impact of learning on sexual selection and speciation

Learning is widespread in nature, occurring in most animal taxa and in several different ecological contexts and, thus, might play a key role in evolutionary processes. Here, we review the accumulating empirical evidence for the involvement of learning in mate choice and the consequences for sexual selection and reproductive isolation. We distinguish two broad categories: learned mate preferences and learned traits under mate selection (such as bird song). We point out that the context of learning, namely how and when learning takes place, often makes a crucial difference to the predicted evolutionary outcome. Factors causing biases in learning and when one should expect the evolution of learning itself are also explored.

Females learn from mothers and males learn from others. The effect of mother and siblings on the development of female mate preferences and male aggression biases in Lake Victoria cichlids, genus Mbipia

While species-assortative behaviour is often observed in sympatrically occurring species, there are few examples where we understand the extent to which development of assortative behaviour is genetically or environmentally determined, for instance, through learning. However, the majority of mate choice theory assumes genetic recognition mechanisms. Knowledge about the development of species recognition is important for our understanding of how closely related species can coexist and how this coexistence may have arisen. The ontogeny of female mate choice, for instance, may critically influence the degree of assortative mating under many circumstances. Also, male assortative aggression behaviour may affect fitness and the possibility for coexistence of two closely related species. Here, we test whether male aggression biases and female mate preferences of two Lake Victoria rock cichlid species, Mbipia mbipi and Mbipia lutea, are affected by experience. With an interspecific cross-fostering experiment, we test for the effect of experience with the phenotype of the mother and that of the siblings on species-assortative mate preferences and aggression biases. We demonstrate that female mate preferences are strongly influenced by learning about their mothers’ phenotype but not by experience with their siblings, despite ample opportunity for interactions. Male aggression biases, in contrast, are affected by experience with siblings but not by learning about their mothers’ phenotype. We suggest that the development of assortative behaviour of females, but not of males, creates favourable conditions for sympatric speciation in Lake Victoria cichlids.

Effects of sensory modality on learned mate preferences in female swordtails

Females often base their mate selection on multiple male traits. Different cues may be weighted differently in mating decisions, and play different roles such as indicating species identity or condition. The ontogeny of preferences for each cue can differ, which may offer a proximate explanation for the differential female evaluation of multimodal traits of males. We investigated whether female preferences for the multimodal male cues of Xiphophorus birchmanni swordtails are learned for traits in both olfactory and visual sensory modalities. We reared X. birchmanni females with either conspecific adults or adults of a closely related species, Xiphophorus malinche. We found that both olfactory and visual preferences were learned, and that the timing of olfactory learning was different from that of visual cues

Song discrimination learning in zebra finches induces highly divergent responses to novel songs.

Perceptual biases can shape the evolution of signal form. Understanding the origin and direction of such biases is therefore crucial for understanding signal evolution. Many animals learn about species-specific signals. Discrimination learning using simple stimuli varying in one dimension (e.g. amplitude, wavelength) can result in perceptual biases with preferences for specific novel stimuli, depending on the stimulus dimensions. We examine how this translates to discrimination learning involving complex communication signals; birdsongs. Zebra finches (Taeniopygia guttata) were trained to discriminate between two artificial songs, using a Go/No-Go procedure. The training songs in experiment 1 differed in the number of repeats of a particular element. The songs in experiment 2 differed in the position of an odd element in a series of repeated elements. We examined generalization patterns by presenting novel songs with more or fewer repeated elements (experiment 1), or with the odd element earlier or later in the repeated element sequence (experiment 2). Control birds were trained with only one song. The generalization curves obtained from (i) control birds, (ii) experimental birds in experiment 1, and (iii) experimental birds in experiment 2 showed large and systematic differences from each other. Birds in experiment 1, but not 2, responded more strongly to specific novel songs than to training songs, showing ‘peak shift’. The outcome indicates that learning about communication signals may give rise to perceptual biases that may drive signal evolution.

Sex differences in developmental plasticity and canalization shape population divergence in mate preferences

Sexual selection of high-quality mates can conflict with species recognition if traits that govern intraspecific mate preferences also influence interspecific recognition. This conflict might be resolved by developmental plasticity and learned mate preferences, which could drive preference divergence in populations that differ in local species composition. We integrate field and laboratory experiments on two calopterygid damselfly species with population genetic data to investigate how sex differences in developmental plasticity affect population divergence in the face of gene flow. Whereas male species recognition is fixed at emergence, females instead learn to recognize heterospecifics. Females are therefore more plastic in their mate preferences than males. We suggest that this results from sex differences in the balance between sexual selection for high-quality mates and selection for species recognition. As a result of these sex differences, females develop more pronounced population divergence in their mate preferences compared with males. Local ecological community context and presence of heterospecifics in combination with sex differences in plasticity and canalization therefore shape population divergence in mate preferences. As ongoing environmental change and habitat fragmentation bring formerly allopatric species into secondary contact, developmental plasticity of mate preferences in either or both sexes might facilitate coexistence and prevent local species extinction.

Divergent hormonal responses to social competition in closely related species of haplochromine cichlid fish.

The diverse cichlid species flocks of the East African lakes provide a classical example of adaptive radiation. Territorial aggression is thought to influence the evolution of phenotypic diversity in this system. Most vertebrates mount hormonal (androgen, glucocorticoid) responses to a territorial challenge. These hormones, in turn, influence behavior and multiple aspects of physiology and morphology. Examining variation in competition-induced hormone secretion patterns is thus fundamental to an understanding of the mechanisms of phenotypic diversification. We test here the hypothesis that diversification in male aggression has been accompanied by differentiation in steroid hormone levels. We studied two pairs of sibling species from Lake Victoria belonging to the genera Pundamilia and Mbipia. The two genera are ecologically differentiated, while sibling species pairs differ mainly in male color patterns. We found that aggression directed toward conspecific males varied between species and across genera: Pundamilia nyererei males were more aggressive than Pundamilia pundamilia males, and Mbipia mbipi males were more aggressive than Mbipia lutea males. Males of both genera exhibited comparable attack rates during acute exposure to a novel conspecific intruder, while Mbipia males were more aggressive than Pundamilia males during continuous exposure to a conspecific rival, consistent with the genus difference in feeding ecology. Variation in aggressiveness between genera, but not between sibling species, was reflected in androgen levels. We further found that M. mbipi displayed lower levels of cortisol than M. lutea. Our results suggest that concerted divergence in hormones and behavior might play an important role in the rapid speciation of cichlid fishes.

Automated Interactive Video Playback for Studies of Animal Communication

Video playback is a widely-used technique for the controlled manipulation and presentation of visual signals in animal communication. In particular, parameter-based computer animation offers the opportunity to independently manipulate any number of behavioral, morphological, or spectral characteristics in the context of realistic, moving images of animals on screen. A major limitation of conventional playback, however, is that the visual stimulus lacks the ability to interact with the live animal. Borrowing from video-game technology, we have created an automated, interactive system for video playback that controls animations in response to real-time signals from a video tracking system. We demonstrated this method by conducting mate-choice trials on female swordtail fish, Xiphophorus birchmanni. Females were given a simultaneous choice between a courting male conspecific and a courting male heterospecific (X. malinche) on opposite sides of an aquarium. The virtual male stimulus was programmed to track the horizontal position of the female, as courting males do in the wild. Mate-choice trials on wild-caught X. birchmanni females were used to validate the prototypes ability to effectively generate a realistic visual stimulus.

Interspecific interactions and learning variability jointly drive geographic differences in mate preferences

Co‐occurrence of closely related species can cause behavioral interference in mating and increase hybridization risk. Theoretically, this could lead to the evolution of more species‐specific mate preferences and sexual signaling traits. Alternatively, females can learn to reject heterospecific males, to avoid male sexual interference from closely related species. Such learned mate discrimination could also affect conspecific mate preferences if females generalize from between species differences to prefer more species‐specific mating signals. Female damselflies of the banded demoiselle (Calopteryx splendens) learn to reject heterospecific males of the beautiful demoiselle (C. virgo) through direct premating interactions. These two species co‐occur in a geographic mosaic of sympatric and microallopatric populations. Whereas C. virgo males have fully melanized wings, male C. splendens wings are partly melanized. We show that C. splendens females in sympatry with C. virgo prefer smaller male wing patches in conspecific males after learning to reject heterospecific males. In contrast, allopatric C. splendens females with experimentally induced experience with C. virgo males did not discriminate against larger male wing patches. Wing patch size might indicate conspecific male quality in allopatry. Co‐occurrence with C. virgo therefore causes females to prefer conspecific male traits that are more species specific, contributing to population divergence and geographic variation in female mate preferences.

The effects of experience on the development of sexual behaviour of males and females of the banded demoiselle (Calopteryx splendens).

Mate preferences can vary in the direction of the preference, as well as the strength of the preference, and both direction and strength of preference are known to be plastic in many species. Preferences might have a learned component, and current and past social context may influence an individuals choosiness. In the damselfly species Calopteryx splendens, females increase the strength of their mate preferences with sexual experience. Here we show that sexually naïve females selectively respond to conspecific courtship as soon as physical contact has been established, suggesting a role for tactile cues perceived through interspecific morphological differences in secondary reproductive traits. In addition our data also shows that males and females selectively respond to the intensity of the courtship of the potential, conspecific mate, while ignoring such information in heterospecific potential mates. These results underscore that mate choice is the result of dynamic interactions between the sexes, where both current and past information are integrated. This article is part of a Special Issue entitled: Cognition in the Wild.

The impact of learned mating traits on speciation is not yet clear: response to Kawecki

In our recent review in TREE [1], we raised the question of how learned traits that act as mating cues can affect the speciation process. In his interesting comment on our paper [2], Kawecki proposes that learning of mating traits or cues can expedite genetic change under directional sexual selection and that, if learning enhances pre-existing genetic variation in a specific population, divergence can ensue. We also refer to theoretical studies that show that learning can facilitate evolution of traits and preferences by sexual selection (and refer to other studies showing that learned traits can also hinder this evolution) [1].