Pau Carazo

Beyond 'nasty neighbours' and 'dear enemies'? Individual recognition by scent marks in a lizard (Podarcis hispanica)

True individual recognition (TIR), the ability to recognize conspecific individuals on the basis of identity cues, is required for the evolution of several social traits (e.g. the maintenance of dominance hierarchies). However, knowledge about the distribution and functional significance of TIR is scant in some vertebrate groups, such as reptiles. In this study we used a functional modification of a habituationedishabituation paradigm to investigate the existence and adaptive significance of TIR in a territorial lizard (Podarcis hispanica, Lacertidae). Males discriminated between individual rivals of similar characteristics (e.g. size, weight, familiarity) solely on the basis of their scent marks. Males also remembered the spatial location of scent marks and subsequently behaved more aggressively towards rival males that consistently marked in the core than on the periphery of their experimental terrarium. Together, these results suggest that, in this species, scent marks function to identify the potential threat posed by each individual neighbour, allowing resident males to allocate their aggressive behaviour accordingly. Our findings challenge the simplistic and commonly held view that ‘dear enemy’ phenomena in lizards are exclusively based on familiarity asymmetries, and support an alternative threat level hypothesis in which TIR may be more important than previously acknowledged.

Chemosensory assessment of rival competitive ability and scent-mark function in a lizard, Podarcis hispanica

Recent studies have stressed the role of scent marks as signals potentially mediating competitor assessment. According to this view, receivers may use scent marks to derive information about the costs of exploiting a given area, but few studies have directly addressed this hypothesis. One of its main predictions is that scent marks should reflect a signaller’s competitive ability. We simulated the situation faced by an intruding male when entering the scent-marked territories of rival males of varying competitive ability to test predictions about the role of scent marks in a lizard, Podarcis hispanica. We report that males were attracted to areas marked by males of similar or higher competitive ability (i.e. larger size), but not to areas scent marked by males of lower competitive ability, and that this preference disappeared towards the end of the breeding season. Our results show that (1) male lizards can assess rival competitive ability (i.e. rival size) on the basis of scent marks alone, (2) scent marks do not function as chemical barriers to deter intruders, and (3) male response to marked areas varies throughout the breeding season, suggesting a shift in the cost-to-benefit balance of entering a scent-marked area. We propose that male assessment of rival competitive ability may function as an indirect assessment mechanism of territory resource quality in this species, and thus that scent marks may convey information not only about costs but also about the benefits of exploiting a scent-marked area.

Chemosensory cues allow male Tenebrio molitor beetles to assess the reproductive status of potential mates

Males of many insect species, including beetles, choose their mates according to their reproductive status. However, the ways in which male beetles evaluate female reproductive status have received little attention. We tested the existence of male mate choice in the mealworm beetle, Tenebrio molitor, by observing mating and courtship behaviour of males given simultaneous access to pairs of females differing in their reproductive status: (1) mature versus immature; (2) virgin versus previously mated; (3) familiar (mated with the experimental male) versus unfamiliar (mated with a different male). Males courted and mated preferentially with mature and virgin females. To determine whether chemical cues played a role in these discriminations, we exposed males to filter paper squares bearing chemical cues from different types of females: (1) virgin versus mated; (2) mature versus immature. Males were significantly more attracted to those squares bearing chemical cues from virgin and mature females, suggesting that males can assess female reproductive status on the basis of chemical cues alone.

Quantity discrimination in Tenebrio molitor: evidence of numerosity discrimination in an invertebrate?

Numerosity discrimination, the ability to distinguish between sets with more and less items, is recognised as the foundation for higher numerical abilities. Understanding numerosity discrimination from a comparative perspective is hence pivotal in tracing the evolution of numerical representation systems. However, numerosity discrimination has been well studied only in vertebrates, where two innate systems of number representation have been described: an ‘analog magnitude system’ used to discriminate among numerosities by representing them as cardinal magnitudes and a ‘parallel individualisation system’ that allows precise discrimination among small arrays of items (≤4) by representing objects individually. We investigated the existence of quantity discrimination in an insect species (Tenebrio molitor) by using a spontaneous two-choice procedure in which males were exposed to substrates bearing odours from different numbers of females (≤4) in increasing numerosity ratios (1:4, 1:3 and 1:2). We show that males can discriminate sources of odours reflecting 1 versus 4 and 1 versus 3 females, but not 2 versus 4 or 1 versus 2, indicating that T. molitor males exhibit a marked preference for sources reflecting more female donors only when numerosity ratios are below 1:2. We discuss the functional significance of this finding and whether our pattern of results could be best explained by summation of a non-numerical continuous variable or by the existence of a numerosity discrimination mechanism with an operational signature ratio of 1:2.

Sex and boldness explain individual differences in spatial learning in a lizard

Understanding individual differences in cognitive performance is a major challenge to animal behaviour and cognition studies. We used the Eastern water skink (Eulamprus quoyii) to examine associations between exploration, boldness and individual variability in spatial learning, a dimension of lizard cognition with important bearing on fitness. We show that males perform better than females in a biologically relevant spatial learning task. This is the first evidence for sex differences in learning in a reptile, and we argue that it is probably owing to sex-specific selective pressures that may be widespread in lizards. Across the sexes, we found a clear association between boldness after a simulated predatory attack and the probability of learning the spatial task. In contrast to previous studies, we found a nonlinear association between boldness and learning: both ‘bold’ and ‘shy’ behavioural types were more successful learners than intermediate males. Our results do not fit with recent predictions suggesting that individual differences in learning may be linked with behavioural types via high–low-risk/reward trade-offs. We suggest the possibility that differences in spatial cognitive performance may arise in lizards as a consequence of the distinct environmental variability and complexity experienced by individuals as a result of their sex and social tactics.

Sexual selection drives asymmetric introgression in wall lizards

Hybridisation is increasingly recognised as an important cause of diversification and adaptation. Here, we show how divergence in male secondary sexual characters between two lineages of the common wall lizard (Podarcis muralis) gives rise to strong asymmetries in male competitive ability and mating success, resulting in asymmetric hybridisation upon secondary contact. Combined with no negative effects of hybridisation on survival or reproductive characters in F1-hybrids, these results suggest that introgression should be asymmetric, resulting in the displacement of sexual characters of the sub-dominant lineage. This prediction was confirmed in two types of secondary contact, across a natural contact zone and in two introduced populations. Our study illustrates how divergence in sexually selected traits via male competition can determine the direction and extent of introgression, contributing to geographic patterns of genetic and phenotypic diversity.

Putting information back into biological communication

At the heart of many debates on communication is the concept of information. There is an intuitive sense in which communication implies the transfer of some kind of information, probably the reason why information is an essential ingredient in most definitions of communication. However, information has also been an endless source of misunderstandings, and recent accounts have proposed that information should be dropped from a formal definition of communication. In this article, we re‐evaluate the merits and the internal logic of information‐based vs. information‐free approaches and conclude that information‐free approaches are conceptually incomplete and operationally hindered. Instead, we propose a functional notion of information that follows logically from previous adaptationist accounts. The ensuing definition of communication provides a wider, more inclusive theoretical scope that reflects more accurately the evolutionary scenario shaping animal signals. Additionally, it is a definition better equipped to deal with the extraordinary diversity of animal signals, facilitates the distinction of honest and deceptive signals at a proximate level and accommodates a number of conceptual and practical issues (e.g. redundancy, alerting components) that are lost when we fail to acknowledge the informative content of animal signals.

Within-group male relatedness reduces harm to females in Drosophila

To resolve the mechanisms that switch competition to cooperation is key to understanding biological organization. This is particularly relevant for intrasexual competition, which often leads to males harming females. Recent theory proposes that kin selection may modulate female harm by relaxing competition among male relatives. Here we experimentally manipulate the relatedness of groups of male Drosophila melanogaster competing over females to demonstrate that, as expected, within-group relatedness inhibits male competition and female harm. Females exposed to groups of three brothers unrelated to the female had higher lifetime reproductive success and slower reproductive ageing compared to females exposed to groups of three males unrelated to each other. Triplets of brothers also fought less with each other, courted females less intensively and lived longer than triplets of unrelated males. However, associations among brothers may be vulnerable to invasion by minorities of unrelated males: when two brothers were matched with an unrelated male, the unrelated male sired on average twice as many offspring as either brother. These results demonstrate that relatedness can profoundly affect fitness through its modulation of intrasexual competition, as flies plastically adjust sexual behaviour in a manner consistent with kin-selection theory.

Colours of quality: structural (but not pigment) coloration informs about male quality in a polychromatic lizard

Chromatic signals result from the differential absorption of light by chemical compounds (pigment-based colours) and/or from differential scattering of light by integument nanostructures (structural colours). Both structural and pigment-based colours can be costly to produce, maintain and display, and have been shown to convey information about a variety of individual quality traits. Male wall lizards, Podarcis muralis, display conspicuously coloured ventral and lateral patches during ritualized inter- and intrasexual displays: ventral colours (perceived as orange, yellow or white by humans) are pigment based, while the ultraviolet (UV)-blue of the outer ventral scales (OVS), located along the flanks, is structurally produced. We used spectrophotometric data from 372 adult males to examine, considering the entire visual spectrum of lizards, whether ventral and OVS colour variables can predict male quality. Results indicate that the hue and UV chroma of OVS are good predictors of fighting ability (size-independent bite force) and body condition, respectively. This suggests that structural colour patches are condition dependent and function as complex multicomponent signals in this species. In contrast, ventral coloration apparently does not function as a male quality indicator. We suggest that ventral and lateral colour patches may be social signals with different information content, possibly aimed at different receivers.

Social behavior, chemical communication, and adult neurogenesis: Studies of scent mark function in Podarcis wall lizards

Lacertid lizards have been hailed as a model system for the study of reptilian chemical communication. However, results obtained with the genus Podarcis, a diverse group of wall lizards with complex systematics, challenge emerging paradigms and caution against hasty generalizations. Here we review the available evidence on the role of chemical stimuli in male-female and male-male interactions in Iberian Podarcis. Males of several species can discriminate between chemicals left on substrates by females of their own or a different species, suggesting that differences in female chemical cues may underlie species recognition in this group. Females, on the other hand, do not respond differentially to conspecific and congeneric male scent marks. Males of Podarcis liolepis use scent marks to recognize rivals individually, evaluate their competitive ability (i.e., body size), and assess the threat posed by each individual rival neighbor. In contrast, females do not exhibit a preference for territories scent marked by larger (i.e., more competitive) males, which suggests a limited role for male scent marks in pre-copulatory mate choice. This behavioral sex difference is consistent with detailed neuro-ethological evidence showing that chemosensory brain areas in P. liolepis are sexually dimorphic. The accessory olfactory bulbs are larger (both in absolute and relative terms) in males than in females, probably as a result of sex-specific rates of adult neurogenesis. In both sexes, cell proliferation undergoes seasonal cycles that may have evolved to satisfy increased chemosensory demands at particular times of the year. Overall, and against recent generalizations, these results suggest that male scent marks have been shaped mainly by strong intrasexual selection.