Mechanistic and experimental analysis of condition and reproduction in a polymorphic lizard

Abstract The importance of genetic and environmental variation in condition in shaping evolutionary trade‐offs have recently been subject to much theoretical discussion, but is very difficult to investigate empirically in most field‐based systems. We present the results from mechanistic experimental manipulations of reproductive investment and condition in two female colour morphs (‘orange’ and ‘yellow’) of side‐blotched lizards (Uta stansburiana). We investigated the interactions between throat colour morphs, condition, local social environment and female survival using path‐analysis. Using follice‐ablation experiments, we show that large clutch size has a negative effect on field survival among yellow females, and that this effect is partly mediated by immunosuppressive effects of large clutches. In orange females these effects were less pronounced, and there was a negative survival effect of strong antibody responses. Hence, we experimentally confirmed our previous findings of correlational selection between female morphotype and immunocompetence, an important condition trait. Manipulation of corticosterone revealed multiple (‘pleiotropic’) direct and indirect effects of this hormone on both condition and reproductive traits. We argue that interaction effects (e.g. between local environments and genotypes) could explain a substantial fraction of variation in condition and reproduction in natural populations. Increased attention to such interaction effects and their fitness consequences will provide novel insights in field studies of selection and reproductive allocation.     

Who is in the neighborhood? Conspecific and heterospecific responses to perceived density for breeding habitat selection

Theoretical models of habitat selection often incorporate negative density dependence. Despite strong negative density‐dependent effects on habitat selection, more recent studies indicate that animals settle near members of their own (conspecific) and other species (heterospecific) when selecting habitat with social cues. Social cue use for habitat selection is particularly common among songbirds, but few studies have investigated if songbirds use social cues to assess conspecific or heterospecific density (as opposed to just presence/absence) when making settlement decisions. We conducted a playback experiment to evaluate if yellow warblers (Setophaga petechia) and willow flycatchers (Empidonax traillii), two potential competitors for breeding habitat, use social cues to assess density (conspecific for warblers and heterospecific for flycatchers) when selecting breeding locations at two spatial scales. We simulated yellow warbler density to be high or low at multiple treatment plots (3.14 ha) with song playback and then evaluated settlement decisions by comparing yellow warbler and willow flycatcher abundances across plots (broad‐scale habitat selection) and individual space use within plots (fine‐scale territory establishment). Yellow warbler density treatments did not affect habitat selection by yellow warblers at the broad scale, but caused individuals to cluster territories at high‐density treatments. Willow flycatchers were most abundant at high‐density treatment plots, but yellow warbler density treatments did not affect territory locations. The results indicate that perceived density affects the habitat selection process for both conspecifics and heterospecifics.     

Similar patterns of frequency‐dependent selection on animal personalities emerge in three species of social spiders

Frequency‐dependent selection is thought to be a major contributor to the maintenance of phenotypic variation. We tested for frequency‐dependent selection on contrasting behavioural strategies, termed here ‘personalities’, in three species of social spiders, each thought to represent an independent evolutionary origin of sociality. The evolution of sociality in the spider genus Anelosimus is consistently met with the emergence of two temporally stable discrete personality types: an ‘aggressive’ or ‘docile’ form. We assessed how the foraging success of each phenotype changes as a function of its representation within a colony. We did this by creating experimental colonies of various compositions (six aggressives, three aggressives and three dociles, one aggressive and five dociles, six dociles), maintaining them in a common garden for 3 weeks, and tracking the mass gained by individuals of either phenotype. We found that both the docile and aggressive phenotypes experienced their greatest mass gain in mixed colonies of mostly docile individuals. However, the performance of both phenotypes decreased as the frequency of the aggressive phenotype increased. Nearly identical patterns of phenotype‐specific frequency dependence were recovered in all three species. Naturally occurring colonies of these spiders exhibit mixtures dominated by the docile phenotype, suggesting that these spiders may have evolved mechanisms to maintain the compositions that maximize the success of the colony without compromising the expected reproductive output of either phenotype.     

Similar preferences for ornamentation in opposite‐ and same‐sex choice experiments

Selection due to social interactions comprises competition over matings (sexual selection stricto sensu) plus other forms of social competition and cooperation. Sexual selection explains sex differences in ornamentation and in various other phenotypes, but does not easily explain cases where those phenotypes are similar in males and females. Understanding such similarities requires knowing how phenotypes influence nonsexual social interactions as well, which can be very important in gregarious animals, but whose role for phenotypic evolution has been overlooked. For example, ‘mate choice’ experiments often found preferences for ornamentation, but have not assessed whether those are strictly sexual or are general social preferences. Using choice experiments with a gregarious and mutually ornamented finch, the common waxbill (Estrilda astrild), we show that preferences for ornamentation in the opposite‐sex also extend to same‐sex interactions. Waxbills discriminated between opposite‐ and same‐sex individuals, but most preferences for colour traits were similar when interacting with either sex. Similar preferences in sexual and nonsexual associations may be widespread in nature, either as social adaptations or as by‐product of mate preferences. In either case, such preferences may set the stage for the evolution of mutual ornamentation and of various other similarities between the sexes.     

Selection for territory acquisition is modulated by social network structure in a wild songbird

The social environment may be a key mediator of selection that operates on animals. In many cases, individuals may experience selection not only as a function of their phenotype, but also as a function of the interaction between their phenotype and the phenotypes of the conspecifics they associate with. For example, when animals settle after dispersal, individuals may benefit from arriving early, but, in many cases, these benefits will be affected by the arrival times of other individuals in their local environment. We integrated a recently described method for calculating assortativity on weighted networks, which is the correlation between an individual's phenotype and that of its associates, into an existing framework for measuring the magnitude of social selection operating on phenotypes. We applied this approach to large‐scale data on social network structure and the timing of arrival into the breeding area over three years. We found that late‐arriving individuals had a reduced probability of breeding. However, the probability of breeding was also influenced by individuals’ social networks. Associating with late‐arriving conspecifics increased the probability of successfully acquiring a breeding territory. Hence, social selection could offset the effects of nonsocial selection. Given parallel theoretical developments of the importance of local network structure on population processes, and increasing data being collected on social networks in free‐living populations, the integration of these concepts could yield significant insights into social evolution.     

Sexual selection in complex communities: Integrating interspecific reproductive interference in structured populations

The social structure of populations plays a key role in shaping variation in sexual selection. In nature, sexual selection occurs in communities of interacting species; however, heterospecifics are rarely included in characterizations of social structure. Heterospecifics can influence the reproductive outcomes of intrasexual competition by interfering with intraspecific sexual interactions (interspecific reproductive interference [IRI]). We outline the need for studies of sexual selection to incorporate heterospecifics as part of the social environment. We use simulations to show that classic predictions for the effect of social structure on sexual selection are altered by an interaction between social structure and IRI. This interaction has wide‐ranging implications for patterns of sexual conflict and kin‐selected reproductive strategies in socially structured populations. Our work bridges the gap between sexual selection research on social structure and IRI, and highlights future directions to study sexual selection in interacting communities.     

Social network structure in wintering golden‐crowned sparrows is not correlated with kinship

Stable social organization in a wide variety of organisms has been linked to kinship, which can minimize conflict due to the indirect fitness benefits from cooperating with relatives. In birds, kin selection has been mostly studied in the context of reproduction or in species that are social year round. Many birds however are migratory, and the role of kinship in the winter societies of these species is virtually unexplored. In a previous study, we discovered striking social complexity and stability in a wintering population of migratory golden‐crowned sparrows (Zonotrichia atricapilla) – individuals repeatedly form close associations with the same social partners, including across multiple winters. Here, we test the possibility that kinship might be involved in these close and stable social affiliations. We examine the relationship between kinship and social structure for two of the consecutive wintering seasons from the previous study. We found no evidence that social structure was influenced by kinship. Relatedness between most pairs of individuals was at most that of first cousins (and mostly far lower). Genetic networks based on relatedness do not correspond to the social networks, and Mantel tests revealed no relationship between kinship and pairwise interaction frequency. Kinship also failed to predict social structure in more fine‐grained analyses, including analyses of each sex separately (in the event that sex‐biased migration might limit kin selection to one sex), and separate analyses for each social community. The complex winter societies of golden‐crowned sparrows appear to be based on cooperative benefits unrelated to kin selection.     

Across‐year social stability shapes network structure in wintering migrant sparrows

Migratory birds often form flocks on their wintering grounds, but important details of social structure such as the patterns of association between individuals are virtually unknown. We analysed networks of co‐membership in short‐term flocks for wintering golden‐crowned sparrows (Zonotrichia atricapilla) across three years and discovered social complexity unsuspected for migratory songbirds. The population was consistently clustered into distinct social communities within a relatively small area (~ 7 ha). Birds returned to the same community across years, with mortality and recruitment leading to some degree of turnover in membership. These spatiotemporal patterns were explained by the combination of space use and social preference – birds that flocked together in one year flocked together again in the subsequent year more often than were expected based on degrees of home range overlap. Our results suggest that a surprising level of social fidelity across years leads to repeatable patterns of social network structure in migratory populations.     

Communicative roots of complex sociality and cognition

Mammals living in more complex social groups typically have large brains for their body size and many researchers have proposed that the primary driver of the increase in brain size through primate and hominin evolution was the selection pressures associated with sociality. Many mammals, and especially primates, use flexible signals that show a high degree of voluntary control and these signals may play an important role in forming and maintaining social relationships between group members. However, the specific role that cognitive skills play in this complex communication, and how in turn this relates to sociality, is still unclear. The hypothesis for the communicative roots of complex sociality and cognition posits that cognitive demands behind the communication needed to form and maintain bonded social relationships in complex social settings drives the link between brain size and sociality. We review the evidence in support of this hypothesis and why key features of cognitively complex communication such as intentionality and referentiality should be more effective in forming and maintaining bonded relationships as compared with less cognitively complex communication. Exploring the link between cognition, communication and sociality provides insights into how increasing flexibility in communication can facilitate the emergence of social systems characterised by bonded social relationships, such as those found in non‐human primates and humans. To move the field forward and carry out both within‐ and among‐species comparisons, we advocate the use of social network analysis, which provides a novel way to describe and compare social structure. Using this approach can lead to a new, systematic way of examining social and communicative complexity across species, something that is lacking in current comparative studies of social structure.     

Vocal culture in New Caledonian crows Corvus moneduloides

While recent research suggests that some animal species may possess ‘cultural’ traditions, much of the current evidence for wild populations remains contentious. This is largely due to the difficulty of demonstrating a fundamental prerequisite for the existence of culture: social learning. As the only case where social learning has been demonstrated conclusively, and subsequently linked to spatial or temporal trait variation, avian vocal dialects are the best studied, and most widely accepted, form of animal culture. Here, we investigate the potential for vocal culture in one of the few animals for which material culture has been suggested: the New Caledonian crow Corvus moneduloides. We show that this species: (1) possesses the capacity for social learning of vocalizations (experimental evidence in the form of a captive subject that reproduces human speech and other anthropogenic noises); and (2) exhibits significant large‐scale, population‐level variation in its vocalizations (cross‐island playback experiments, with analyses controlling for a substantial set of potentially confounding variables). In combination, this provides strong evidence for the existence of ‘culture’ in these birds. More specifically, our findings reveal that the species exhibits sufficient social learning mechanisms, and within‐population structuring, to generate and perpetuate cultural variation in at least one behavioural domain. This is a critical first step towards demonstrating cultural transmission in other behaviours, including tool manufacture and tool use, opening the door for the simultaneous investigation of vocal and material culture in a nonhuman species. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2010, 101 , 767–776.     

The socio‐genetics of a complex society: female gelada relatedness patterns mirror association patterns in a multilevel society

Multilevel societies with fission–fusion dynamics—arguably the most complex animal societies—are defined by two or more nested levels of organization. The core of these societies are modular social units that regularly fission and fuse with one another. Despite convergent evolution in disparate taxa, we know strikingly little about how such societies form and how fitness benefits operate. Understanding the kinship structure of complex societies could inform us about the origins of the social structure as well as about the potential for individuals in these societies to accrue indirect fitness benefits. Here, we combined genetic and behavioural data on geladas (Theropithecus gelada), an Old World Monkey, to complete the most comprehensive socio‐genetic analysis of a multilevel society to date. In geladas, individuals in the core social ‘units’, associate at different frequencies to form ‘teams’, ‘bands’ and, the largest aggregations, ‘communities’. Units were composed of closely related females, and females remained with their close kin during permanent fissions of units. Interestingly, female–female relatedness also significantly predicted between‐unit, between‐team and between‐band association patterns, while male–male relatedness did not. Thus, it is likely that the socio‐genetic structure of gelada society results from females maintaining associations with their female relatives during successive unit fissions—possibly in an attempt to balance the direct and indirect fitness benefits of group living. Overall, the persistence of associations among related females across generations appears to drive the formation of higher levels of gelada society, suggesting that females seek kin for inclusive fitness benefits at multiple levels of gelada society.     

Social traits,social networks and evolutionary biology

The social environment is both an important agent of selection for most organisms, and an emergent property of their interactions. As an aggregation of interactions among members of a population, the social environment is a product of many sets of relationships and so can be represented as a network or matrix. Social network analysis in animals has focused on why these networks possess the structure they do, and whether individuals’ network traits, representing some aspect of their social phenotype, relate to their fitness. Meanwhile, quantitative geneticists have demonstrated that traits expressed in a social context can depend on the phenotypes and genotypes of interacting partners, leading to influences of the social environment on the traits and fitness of individuals and the evolutionary trajectories of populations. Therefore, both fields are investigating similar topics, yet have arrived at these points relatively independently. We review how these approaches are diverged, and yet how they retain clear parallelism and so strong potential for complementarity. This demonstrates that, despite separate bodies of theory, advances in one might inform the other. Techniques in network analysis for quantifying social phenotypes, and for identifying community structure, should be useful for those studying the relationship between individual behaviour and group‐level phenotypes. Entering social association matrices into quantitative genetic models may also reduce bias in heritability estimates, and allow the estimation of the influence of social connectedness on trait expression. Current methods for measuring natural selection in a social context explicitly account for the fact that a trait is not necessarily the property of a single individual, something the network approaches have not yet considered when relating network metrics to individual fitness. Harnessing evolutionary models that consider traits affected by genes in other individuals (i.e. indirect genetic effects) provides the potential to understand how entire networks of social interactions in populations influence phenotypes and predict how these traits may evolve. By theoretical integration of social network analysis and quantitative genetics, we hope to identify areas of compatibility and incompatibility and to direct research efforts towards the most promising areas. Continuing this synthesis could provide important insights into the evolution of traits expressed in a social context and the evolutionary consequences of complex and nuanced social phenotypes.     

What's your move? Movement as a link between personality and spatial dynamics in animal populations

Recent studies have established the ecological and evolutionary importance of animal personalities. Individual differences in movement and space‐use, fundamental to many personality traits (e.g. activity, boldness and exploratory behaviour) have been documented across many species and contexts, for instance personality‐dependent dispersal syndromes. Yet, insights from the concurrently developing movement ecology paradigm are rarely considered and recent evidence for other personality‐dependent movements and space‐use lack a general unifying framework. We propose a conceptual framework for personality‐dependent spatial ecology. We link expectations derived from the movement ecology paradigm with behavioural reaction‐norms to offer specific predictions on the interactions between environmental factors, such as resource distribution or landscape structure, and intrinsic behavioural variation. We consider how environmental heterogeneity and individual consistency in movements that carry‐over across spatial scales can lead to personality‐dependent: (1) foraging search performance; (2) habitat preference; (3) home range utilization patterns; (4) social network structure and (5) emergence of assortative population structure with spatial clusters of personalities. We support our conceptual model with spatially explicit simulations of behavioural variation in space‐use, demonstrating the emergence of complex population‐level patterns from differences in simple individual‐level behaviours. Consideration of consistent individual variation in space‐use will facilitate mechanistic understanding of processes that drive social, spatial, ecological and evolutionary dynamics in heterogeneous environments.     

Oh sister,where art thou? Spatial population structure and the evolution of an altruistic defence trait

The evolution of parasite virulence and host defences is affected by population structure. This effect has been confirmed in studies focusing on large spatial scales, whereas the importance of local structure is not well understood. Slavemaking ants are social parasites that exploit workers of another species to rear their offspring. Enslaved workers of the host species Temnothorax longispinosus have been found to exhibit an effective post‐enslavement defence behaviour: enslaved workers were observed killing a large proportion of the parasites’ offspring. As enslaved workers do not reproduce, they gain no direct fitness benefit from this ‘rebellion’ behaviour. However, there may be an indirect benefit: neighbouring host nests that are related to ‘rebel’ nests can benefit from a reduced raiding pressure, as a result of the reduction in parasite nest size due to the enslaved workers’ killing behaviour. We use a simple mathematical model to examine whether the small‐scale population structure of the host species could explain the evolution of this potentially altruistic defence trait against slavemaking ants. We find that this is the case if enslaved host workers are related to nearby host nests. In a population genetic study, we confirm that enslaved workers are, indeed, more closely related to host nests within the raiding range of their resident slavemaker nest, than to host nests outside the raiding range. This small‐scale population structure seems to be a result of polydomy (e.g. the occupation of several nests in close proximity by a single colony) and could have enabled the evolution of ‘rebellion’ by kin selection.     

Morphological effects of transcardially perfused SDS on the rat brain

Background information. For explanation of the formation of ‘dark’ neurons, an enigmatic phenomenon in neuropathology, we hypothesized recently that all spaces between the ultrastructural elements visible in the traditional transmission electron microscope are filled with a gel structure that stores free energy in the form of non‐covalent interactions, is continuous in the whole soma—dendrite domains of neurons, and is capable of whole‐cell phase transition. This hypothesis was deduced from the fact that ‘dark’ neurons can be formed, even under conditions extremely unfavourable for enzyme‐mediated biochemical processes, if initiated by a physical damage. In order to gain further information on this gel structure, we perfused transcardially rats for 5 min with physiological saline containing 1 mM SDS before the perfusion of a fixative for electron microscopy. Results. Dramatic compaction of visibly intact ultrastructural elements was caused in the whole soma—dendrite domains of thinly scattered neurons (‘dark’ neurons), whereas substantial cytoplasmic swelling and patchy ultrastructural disintegration occurred in numerous other neurons (‘light’ neurons). Similar morphological changes were observed in scattered astrocytes, oligodendrocytes, pericytes and endothelial cells. Conclusions. These observations: (i) support the existence of the above intracellular gel structure in neurons; (ii) allow the conclusion that this gel structure is present in the form of an ubiquitous trabecular network surrounded by a confluent system of fluid cytoplasm; (iii) draw attention to the possibility that the previous two statements also apply to other cell types of the brain tissue; and (iv) suggest that pressure‐induced direct channels exist between neurons and astrocytes.     

Display Plasticity in Response to a Robotic Lizard: Signal Matching or Song Sharing in Lizards?

Many territorial songbirds alter the structure of their songs after listening to and interacting repeatedly with the same neighbors. Here, we use a robotic lizard to test for similar learned changes in signal structure in male Sagebrush lizards, Sceloporus graciosus. Subjects were exposed to two types of headbob displays (species‐typical and unusual) both in short‐term tests and in repeated exposures for 10 d. We found no evidence for immediate changes in signal structure to match a particular opponent (signal matching) or long‐term changes after repeated exposure (‘song’ sharing). If anything, the lizards’ displays became less like that of the robotic stimulus over time. Further tests of other taxa are needed to identify the evolutionary forces that lead to these forms of behavioral plasticity and to determine whether song sharing and signal matching are unique characteristic of songbirds. Lizards also became more agitated and produced more highly aggressive displays of their own when confronted with headbob displays that violated the basic syntactic structure of their display system, confirming that they were paying attention to subtle differences in display structure despite the artificial nature of the treatments. Thus, our study also adds to the growing evidence supporting the use of robotic playbacks to study animal communication.     

Pervasive,yet idiosyncratic,epistatic pleiotropy during adaptation in a behaviourally complex microbe

Understanding how multiple mutations interact to jointly impact multiple ecologically important traits is critical for creating a robust picture of organismal fitness and the process of adaptation. However, this is complicated by both environmental heterogeneity and the complexity of genotype‐to‐phenotype relationships generated by pleiotropy and epistasis. Moreover, little is known about how pleiotropic and epistatic relationships themselves change over evolutionary time. The soil bacterium Myxococcus xanthus employs several distinct social traits across a range of environments. Here, we use an experimental lineage of M. xanthus that evolved a novel form of social motility to address how interactions between epistasis and pleiotropy evolve. Specifically, we test how mutations accumulated during selection on soft agar pleiotropically affect several other social traits (hard agar motility, predation and spore production). Relationships between changes in swarming rate in the selective environment and the four other traits varied greatly over time in both direction and magnitude, both across timescales of the entire evolutionary lineage and individual evolutionary time steps. We also tested how a previously defined epistatic interaction is pleiotropically expressed across these traits. We found that phenotypic effects of this epistatic interaction were highly correlated between soft and hard agar motility, but were uncorrelated between soft agar motility and predation, and inversely correlated between soft agar motility and spore production. Our results show that ‘epistatic pleiotropy’ varied greatly in magnitude, and often even in sign, across traits and over time, highlighting the necessity of simultaneously considering the interacting complexities of pleiotropy and epistasis when studying the process of adaptation.     

Capturing the superorganism: a formal theory of group adaptation

Adaptation is conventionally regarded as occurring at the level of the individual organism. However, in recent years there has been a revival of interest in the possibility for group adaptations and superorganisms. Here, we provide the first formal theory of group adaptation. In particular: (1) we clarify the distinction between group selection and group adaptation, framing the former in terms of gene frequency change and the latter in terms of optimization; (2) we capture the superorganism in the form of a ‘group as maximizing agent’ analogy that links an optimization program to a model of a group‐structured population; (3) we demonstrate that between‐group selection can lead to group adaptation, but only in rather special circumstances; (4) we provide formal support for the view that between‐group selection is the best definition for ‘group selection’; and (5) we reveal that mechanisms of conflict resolution such as policing cannot be regarded as group adaptations.     

The correlation between coloration and exploration behaviour varies across hierarchical levels in a wild passerine bird

In vertebrates, darker individuals are often found to be more active and willing to take risks (representing characteristics of a ‘proactive’ coping style), whereas lighter individuals are instead more cautious and less active (representing characteristics of a ‘reactive’ coping style). It is thus generally expected that melanin‐based coloration and proactivity form a suite of positively integrated traits at the among‐individual level. Here, we use a multigenerational pedigree of free‐living great tits (Parus major) to partition variation in, and the correlation between, melanin‐based breast stripe (‘tie’) size and exploration behaviour (a proxy for coping style) into its among‐ and within‐individual components. We show that both traits harbour heritable variation. Against predictions, tie size and speed of exploration were negatively correlated at the among‐individual level due to the combined influences of permanent environmental and additive genetic effects. By contrast, the two traits were weakly positively correlated within individuals (i.e. individuals increasing in tie size after moult tended to become more explorative). The patterns of among‐individual covariance were not caused by correlational selection as we found additive and opposite selection pressures acting on the two traits. These findings imply that testing hypotheses regarding the existence of a ‘syndrome’ at the among‐individual level strictly requires variance partitioning to avoid inappropriate interpretations as the negative ‘unpartitioned’ phenotypic correlation between exploration and tie size resulted from counteracting effects of within‐ and among‐individual correlations. Identifying sources and levels of (co)variation in phenotypic traits is thus critical to our understanding of biological patterns and evolutionary processes.     

Unravelling the Philosophies Underlying ‘Animal Personality’ Studies: A Brief Re‐Appraisal of the Field

The last decade has seen lots of studies on ‘animal personality’ (i.e. the study of consistent between‐individual behavioural differences). As timely and promising as this field is, its development has come with a diversity of research questions. As an unfortunate consequence, it now suffers from substantial confusion about what ‘animal personality’ is, and how relevant related research frameworks are. Here, we stress the current inconsistencies and sources of confusion pertaining to the field, and their consequences on terminology used and miscommunication between researchers. In an attempt to unravel and clarify the concepts underlying the field, we identify two distinct, but complementary, theory‐driven conceptual frameworks: the intra‐individual variability (IIV) approach and the life‐history (LH) approach, which we believe encompass the vast majority of existing ‘personality studies’. Finally, we argue in favour of theory‐driven studies of consistent behavioural differences and state that the integrative statistical properties of random regression models should not override the merit of alternative conceptual frameworks. We then provide brief guidelines and warnings for a parsimonious and sound use of terminology.