Understanding the evolution of personality requires the study of mechanisms behind the development and life history of personality traits.

Research on animal personality explains the coexistence of distinct behavioural phenotypes within a species and demonstrates limits to individual plasticity. However, the mechanisms guiding the lifelong development of personality should receive more attention, because many elements of personality are emergent properties of interactions between the environment and an individual's genetic background. In these interactions, mechanisms (e.g. genetic regulatory networks, epigenetic processes and neuroendocrine regulation) influencing personality may be modified. An approach integrating proximate mechanisms with a view of lifelong personality development will crucially improve understanding stability, plasticity and inter-individual variability of personalities and clarify the effects of selection on the phenomenon.

Hybridization masks speciation in the evolutionary history of the Galápagos marine iguana.

The effects of the direct interaction between hybridization and speciation-two major contrasting evolutionary processes--are poorly understood. We present here the evolutionary history of the Galápagos marine iguana (Amblyrhynchus cristatus) and reveal a case of incipient within--island speciation, which is paralleled by between-island hybridization. In-depth genome-wide analyses suggest that Amblyrhynchus diverged from its sister group, the Galápagos land iguanas, around 4.5 million years ago (Ma), but divergence among extant populations is exceedingly young (less than 50,000 years). Despite Amblyrhynchus appearing as a single long-branch species phylogenetically, we find strong population structure between islands, and one case of incipient speciation of sister lineages within the same island--ostensibly initiated by volcanic events. Hybridization between both lineages is exceedingly rare, yet frequent hybridization with migrants from nearby islands is evident. The contemporary snapshot provided by highly variable markers indicates that speciation events may have occurred throughout the evolutionary history of marine iguanas, though these events are not visible in the deeper phylogenetic trees. We hypothesize that the observed interplay of speciation and hybridization might be a mechanism by which local adaptations, generated by incipient speciation, can be absorbed into a common gene pool, thereby enhancing the evolutionary potential of the species as a whole.

Differences in foraging ecology align with genetically divergent ecotypes of a highly mobile marine top predator.

Foraging differentiation within a species can contribute to restricted gene flow between ecologically different groups, promoting ecological speciation. Galapagos sea lions (Zalophus wollebaeki) show genetic and morphological divergence between the western and central archipelago, possibly as a result of an ecologically mediated contrast in the marine habitat. We use global positioning system (GPS) data, time-depth recordings (TDR), stable isotope and scat data to compare foraging habitat characteristics, diving behaviour and diet composition of Galapagos sea lions from a western and a central colony. We consider both juvenile and adult life stages to assess the potential role of ontogenetic shifts that can be crucial in shaping foraging behaviour and habitat choice for life. We found differences in foraging habitat use, foraging style and diet composition that aligned with genetic differentiation. These differences were consistent between juvenile and adult sea lions from the same colony, overriding age-specific behavioural differences. Our study contributes to an understanding of the complex interaction of ecological condition, plastic behavioural response and genetic make-up of interconnected populations.

Divergent allele advantage at MHC-DRB through direct and maternal genotypic effects and its consequences for allele pool composition and mating.

It is still debated whether main individual fitness differences in natural populations can be attributed to genome-wide effects or to particular loci of outstanding functional importance such as the major histocompatibility complex (MHC). In a long-term monitoring project on Galápagos sea lions (Zalophus wollebaeki), we collected comprehensive fitness and mating data for a total of 506 individuals. Controlling for genome-wide inbreeding, we find strong associations between the MHC locus and nearly all fitness traits. The effect was mainly attributable to MHC sequence divergence and could be decomposed into contributions of own and maternal genotypes. In consequence, the population seems to have evolved a pool of highly divergent alleles conveying near-optimal MHC divergence even by random mating. Our results demonstrate that a single locus can significantly contribute to fitness in the wild and provide conclusive evidence for the 'divergent allele advantage' hypothesis, a special form of balancing selection with interesting evolutionary implications.

Same size--same niche? Foraging niche separation between sympatric juvenile Galapagos sea lions and adult Galapagos fur seals.

1. In vertebrates, patterns of resource utilization change throughout development according to age- and or size-specific abilities and requirements. Thus, interspecific competition affects different age classes differently. 2. Adults of sympatric species often show distinct foraging niche segregation, but juvenile resource use might overlap with adult competitors of similar body size. Resultant negative effects on juveniles can have important consequences for population dynamics, yet such interactions have received little attention in studies of mammalian communities. 3. Using GPS tracking devices, time-depth recorders and stable isotope data, we compared diving depth, activity time, trophic position and foraging habitat characteristics to investigate foraging niche overlap between similar-sized sympatric juvenile Galapagos sea lions (Zalophus wollebaeki) and adult Galapagos fur seals (Arctocephalus galapagoensis) and compared each group with much larger-bodied adult Galapagos sea lions. 4. We found little indication for direct competition but a complex pattern of foraging niche segregation: juvenile sea lions and adult fur seals dived to shallow depths at night, but foraged in different habitats with limited spatial overlap. Conversely, juvenile and adult sea lions employed different foraging patterns, but their foraging areas overlapped almost completely. 5. Consistency of foraging habitat characteristics between juvenile and adult sea lions suggests that avoidance of competition may be important in shaping foraging habitat utilization. Resultant specialization on a limited habitat could contribute to low sea lion numbers that contrast with high fur seal abundance. Our data suggest that exploitation by multiple predators within spatially restricted foraging ranges of juveniles might negatively impact juvenile foraging success and ultimately influence population dynamics.

Shifts in energy allocation and reproduction in response to temperature in a small precocial mammal.

BACKGROUND: Species adjust to changes in temperature and the accompanying reduction in resource availability during the annual cycle by shifts in energy allocation. As it gets colder, the priority of energy allocation to maintenance increases and reproduction is reduced or abandoned. RESULTS: We studied whether and how young female guinea pigs (Cavia porcellus) adjust even under ad libitum food conditions growth, storage of fat reserves and reproduction when kept at 5 °C versus 15 °C, and how offspring born into these conditions compensate during development to independence. Reproducing females grew less in the cold. Their lower weight resulted largely from less fat storage whereas growth in fat free mass was about the same for both groups. The increased need for thermoregulation diminished fat storage most likely due to the development of more brown fat tissue. Reproductive activity did not differ between groups in terms of litter frequency, mass and size. However, females in 5 °C weaned pups later (around day 25) than females in 15 °C (around day 21). Later weaning did not make up for the higher energy expenditure of pups in cold conditions leading to slower growth and less fat storage. Female pups born into the cold matured later than those born in 15 °C. Investment in reproduction continued but allocation to individual pups declined. CONCLUSIONS: In more thermally demanding conditions female guinea pigs - even under ad libitum food abundance - transfer the higher costs of maintenance and reproduction largely to offspring.

A stable foraging polymorphism buffers Galápagos sea lions against environmental change.

Understanding the ability of animals to cope with a changing environment is critical in a world affected by anthropogenic disturbance.1 Individual foraging strategies may influence the coping ability of entire populations, as these strategies can be adapted to contrasting conditions, allowing populations with foraging polymorphisms to be more resilient toward environmental change.2,3 However, environmentally dependent fitness consequences of individual foraging strategies and their effects on population dynamics have not been conclusively documented.4,5 Here, we use biologging data from endangered Galápagos sea lion females (Zalophus wollebaeki) to show that benthically foraging individuals dig after sand-dwelling prey species while pelagic foragers hunt in more open waters. These specialized foraging behaviors result in distinct and temporally stable patterns of vibrissae abrasion. Using vibrissae length as a visual marker for the benthic versus pelagic foraging strategies, we furthermore uncovered an environment-dependent fitness trade-off between benthic and pelagic foragers, suggesting that the foraging polymorphism could help to buffer the population against the negative effects of climate change. However, demographic projections suggest that this buffering effect is unlikely to be sufficient to reverse the ongoing population decline of the past four decades.6 Our study shows how crucial a deeper understanding of behavioral polymorphisms can be for predicting how populations cope within a rapidly changing world. VIDEO ABSTRACT.

The emergence of personality in animals: the need for a developmental approach.

Interest has been growing among behavioral biologists in individual differences in animal behavior of the kind that can be considered to reflect differences in personality. Once considered the exclusive domain of human psychology, biologists have found evidence for personality across a wide range of species, while behavioral ecologist and theoretical biologists recognize the likely evolutionary origins and contribution to fitness of such. However, until recently most work has concentrated on ultimate questions of fitness and thus on adult animals, with little attention given to proximate, developmental origins. This is now changing, as approaches to studying animal personality broaden and methodologies are developed enabling this to be studied across periods of near continuous and often rapid ontogenetic change. Debate continues, however, about the right methodologies to characterize the phenomenon and attempt to do so in a comparable manner across taxa that differ as widely in the expression of "personality" as insects and mammals. This makes it necessary to discuss this field in an interdisciplinary context among psychologists and biologists, and was the rational for a meeting on "The Emergence of Personality in Animals" held in May 2010 at the Center for Interdisciplinary Research (Zentrum für Interdisziplinäre Forschung; ZiF), Bielefeld, Germany. The diversity of topics, viewpoints and organisms covered and the excitement created by the ensuing discussions is reflected in the resulting collection of papers forming this special issue.

Unfolding personalities: the importance of studying ontogeny.

We aim to stimulate an ontogenetic approach to personalities. We explain the importance of studying development for understanding proximate and ultimate aspects of personality and critically discuss, partly by perhaps provocative statements, our current lack of knowledge and potential approaches to the study of personality development. We first clarify some terminology and argue for a difference between behavioral profiles (BP; at the descriptive level) and personality (at the explanatory level). We then focus on the issue of temporal stability of personality, arguing that based on evolutionary theory, neurophysiological knowledge, and recent findings, personality is probably less stable than often thought. Next we consider the potential influence of genes, discussing gene by environment correlations and interactions and argue that developmental changes in the regulation of DNA expression are probably more relevant than individual differences in DNA sequence. We end by suggesting perspectives for future research.

Cooperation and opportunism in Galapagos sea lion hunting for shoaling fish.

For predators, cooperation can decrease the cost of hunting and potentially augment the benefits. It can also make prey accessible that a single predator could not catch. The degree of cooperation varies substantially and may range from common attraction to a productive food source to true cooperation involving communication and complementary action by the individuals involved. We here describe cooperative hunting of Galapagos sea lions (Zalophus wollebaeki) for Amberstripe scad (Decapterus muroadsi), a schooling, fast swimming semipelagic fish. A group of 6-10 sea lions, usually females only, drove scad over at least 600-800 m from open water into a cove where, in successful hunts, they drove them ashore. Frequently, these "core hunters" were joined toward the final stages of the hunt by another set of opportunistic sea lions from a local colony at that beach. The "core hunters" did not belong to that colony and apparently were together coming toward the area specifically for the scad hunt. Based on the observation of 40 such hunts from 2016 to 2020, it became evident that the females performed complementary actions in driving the scad toward the cove. No specialization of roles in the hunt was observed. All "core hunters" and also opportunistically joining sea lions from the cove shared the scad by randomly picking up a few of the 25-300 (mean 100) stranded fish as did scrounging brown pelicans. In one of these hunts, four individual sea lions were observed to consume 7-8 fish each in 25 s. We conclude that the core hunters must communicate about a goal that is not present to achieve joint hunting but presently cannot say how they do so. This is a surprising achievement for a species that usually hunts singly and in which joint hunting plays no known role in the evolution of its sociality.

Male reproductive success and its behavioural correlates in a polygynous mammal, the Galápagos sea lion (Zalophus wollebaeki).

Sexual selection theory predicts competitive males and choosy females. Nevertheless, since molecular marker-based studies, paternity outside the expected mating patterns has increasingly been described. Even in highly polygynous systems, where paternity is expected to be strongly skewed towards large, dominant males, alternative mating tactics have been suggested. We examined reproductive success in the polygynous Galápagos sea lion (Zalophus wollebaeki). Semiaquatic territoriality allows females to move freely and may lower the degree of polygyny otherwise suggested by both territorial behaviour and strong sexual dimorphism. We assigned paternities with 22 microsatellites and analysed how male reproductive success was related to size, dominance status, intra-sexual agonistic behaviour, proximity to females, and attendance in the colony. Male behaviour was consistent across two seasons for all parameters under consideration. Attendance was by far the most important determinant of paternal success. Skew in reproductive success towards large, dominant males was weak and dominance status played no role. This appears to be caused by an extremely long reproductive season lasting five or more months, making it difficult for any male to monopolize receptive females. Females seem to choose displaying males that were present in the colony for a long time rather than dominance per se. Sexual dimorphism in Galápagos sea lions may thus be more influenced by selection for fasting than fighting ability. Our data provide further evidence for alternative mating tactics, as several males gained relatively high reproductive success despite short attendance and hardly any involvement in agonistic interactions.

Within-Family Environment and Cross-Fostering Stress Affect Behavior and Physiology in Wild Cavies (Cavia aperea).

Stability of personality traits is well-documented for a wide variety of animals. However, previous results also suggest that behavioral phenotypes are plastic during early ontogeny and can be adaptively shaped to the social environment. In cavies (Cavia aperea), it has already been documented that the size at birth relative to siblings (size rank) greatly influences various behavioral and physiological traits that last at least until independence. The aim of the current study was (1) to investigate if behavioral and physiological differences between pups of the same litter persist until after independence and influence development long-lasting, (2) to determine the potential plasticity in response to changes in the early within-family environment by cross-fostering pups either to the same, a lower, or a higher size rank in a foster-family. We measured three behavioral traits (number of interactions with a novel object, distance moved in an open field, struggle docility) and two physiological traits (resting metabolic rate and basal cortisol levels). We predicted that cross-fostering into a litter where pups occupy the same size rank would not change the expression of traits. Cross-fostering to a different size rank should not influence the expression of traits if repeatability measures indicate low plasticity. Alternatively, if the traits are plastic, animals should adjust trait expression to fit with the size rank occupied in the foster litter. Initial differences in struggle docility, distance moved in an open field and in baseline cortisol concentration between pups of different size-ranks did not remain stable beyond independence. In addition, we found remarkable plasticity of the measured traits in response to cross-fostering to the same, a smaller or larger size-rank, suggesting that differences between pups are more the result of social constraints leading to adaptive shaping of individual phenotypes within a family. We also found a significant influence of the cross-fostering procedure itself. Cross-fostered individuals were less bold, grew slower and showed elevated resting metabolic rates. This finding suggests a cautious interpretation of previous cross-fostering studies and stresses the need for proper control groups to reliably separate the effect of cross-fostering per se from those induced by an experimental treatment.

Reproduction affects immune defenses in the guinea pig even under ad libitum food.

Reproduction is one of the costliest processes in the life of an animal. Life history theory assumes that when resources are limiting allocation to reproduction will reduce allocation to other essential processes thereby inducing costs of reproduction. The immune system is vital for survival. If reproduction reduces investment in immune function, this could increase the risk of disease, morbidity and mortality. We here test in the guinea pig, if even under ad libitum food conditions, pregnancy and lactation reduce the activity of the adaptive and innate immune system compared to the reaction of non-reproducing animals. In response to a challenge with keyhole limpet haemocyanin the antibody-mediated adaptive immunity during (pregnancy and) lactation was reduced. Pregnant and lactating females showed higher levels of bacterial killing activity, an integrated measure of innate immunity, than non-reproducing females. However, two major effectors of the innate immunity, the natural antibody and the complement of pregnant and lactating females showed lower levels than in non-reproducing females. Pregnant and lactating females did not differ significantly in the expressed levels of innate immunity. Our results indicate that changes in the immune response during reproduction are physiological adjustments to predictable allocation problems, because they happen even under ad libitum food availability.

Puberty in female cavies (Cavia aperea) is affected by photoperiod and social conditions.

In many environments, photoperiod is a reliable predictor of ecological conditions. Such predictability generally declines towards low latitudes as the yearly cycle becomes less marked. It has been claimed that photoperiodic effects are small in cavies and guinea pigs that reproduce throughout the year. We here investigated photoperiodic influences on the onset of puberty in female cavies (Cavia aperea) and show that photoperiod exerts a major influence. Female pups kept in groups of two matured at about 47 days when born into lengthening (from 10:14 to 12.5:11.5 L:D) and 79 days when born into shortening day length (from 14.5:9.5 to 12:12 L:D) and kept under identical short day conditions after weaning on day 20 of life (12.25:11.75 L:D). As shown previously, social conditions, especially the presence of an adult male, proved important modifiers of the onset of maturity in females. Differential stress cannot be responsible for the social effects on puberty as social conditions did not affect cortisol levels in young females. We conclude that photoperiod plays an important role in gearing the onset of cavy reproduction to the seasons and that specific male stimuli rather than unspecific effects of stressors accelerate female maturation.

Senescence and costs of reproduction in the life history of a small precocial species.

Species following a fast life history are expected to express fitness costs mainly as increased mortality, while slow-lived species should suffer fertility costs. Because observational studies have limited power to disentangle intrinsic and extrinsic factors influencing senescence, we manipulated reproductive effort experimentally in the cavy (Cavia aperea) which produces extremely precocial young. We created two experimental groups: One was allowed continuous reproduction (CR) and the other intermittent reproduction (IR) by removing males at regular intervals. We predicted that the CR females should senesce (and die) earlier and produce either fewer and/or smaller, slower growing offspring per litter than those of the IR group. CR females had 16% more litters during three years than IR females. CR females increased mass and body condition more steeply and both remained higher until the experiment ended. Female survival showed no group difference. Reproductive senescence in litter size, litter mass, and reproductive effort (litter mass/maternal mass) began after about 600 days and was slightly stronger in CR than IR females. Litter size, litter mass, and offspring survival declined with maternal age and were influenced by seasonality. IR females decreased reproductive effort less during cold seasons and only at higher age than CR females. Nevertheless, offspring winter mortality was higher in IR females. Our results show small costs of reproduction despite high reproductive effort, suggesting that under ad libitum food conditions costs depend largely on internal regulation of allocation decisions.

Evolution of age at primiparity in pinnipeds in the absence of the quality-quantity trade-off in reproduction.

Age at primiparity (AP) is a key life history trait which is crucial to the evolution of life history strategies. This trait is particularly interesting in pinnipeds (walrus, eared seals, and true seals), which are monotocous animals. Thus, the commonly observed trade-off between offspring quality and quantity does not apply to this taxon. Therefore, comparative studies on the evolution of AP might shed light on other important evolutionary correlates when litter size is fixed. Using phylogenetic generalized least squares analyses, we found a strong negative and robust correlation between relative birth mass (mean pup birth mass as a proportion of mean adult female mass) and AP. Rather than trading-off an early start of reproduction with light relative offspring mass, this result suggests that pinnipeds exhibit either faster (i.e., higher relative offspring mass leading to shorter lactation length, and thus shorter interbirth interval) or slower life histories and that an early AP and a heavy relative offspring mass co-evolved into a comparatively fast life history strategy. On the other hand, AP was positively related to lactation length: A later start of reproduction was associated with a longer lactation length. Consequently, variation in AP in pinnipeds seems to be affected by an interplay between costs and benefits of early reproduction mediated by relative investment into the single offspring via relative birth mass and lactation length.

Tracing early stages of species differentiation: ecological, morphological and genetic divergence of Galápagos sea lion populations.

BACKGROUND: Oceans are high gene flow environments that are traditionally believed to hamper the build-up of genetic divergence. Despite this, divergence appears to occur occasionally at surprisingly small scales. The Galápagos archipelago provides an ideal opportunity to examine the evolutionary processes of local divergence in an isolated marine environment. Galápagos sea lions (Zalophus wollebaeki) are top predators in this unique setting and have an essentially unlimited dispersal capacity across the entire species range. In theory, this should oppose any genetic differentiation. RESULTS: We find significant ecological, morphological and genetic divergence between the western colonies and colonies from the central region of the archipelago that are exposed to different ecological conditions. Stable isotope analyses indicate that western animals use different food sources than those from the central area. This is likely due to niche partitioning with the second Galápagos eared seal species, the Galápagos fur seal (Arctocephalus galapagoensis) that exclusively dwells in the west. Stable isotope patterns correlate with significant differences in foraging-related skull morphology. Analyses of mitochondrial sequences as well as microsatellites reveal signs of initial genetic differentiation. CONCLUSION: Our results suggest a key role of intra- as well as inter-specific niche segregation in the evolution of genetic structure among populations of a highly mobile species under conditions of free movement. Given the monophyletic arrival of the sea lions on the archipelago, our study challenges the view that geographical barriers are strictly needed for the build-up of genetic divergence. The study further raises the interesting prospect that in social, colonially breeding mammals additional forces, such as social structure or feeding traditions, might bear on the genetic partitioning of populations.

Kin in space: social viscosity in a spatially and genetically substructured network.

Population substructuring is a fundamental aspect of animal societies. A growing number of theoretical studies recognize that who-meets-whom is not random, but rather determined by spatial relationships or illustrated by social networks. Structural properties of large highly dynamic social systems are notoriously difficult to unravel. Network approaches provide powerful ways to analyse the intricate relationships between social behaviour, dispersal strategies and genetic structure. Applying network analytical tools to a colony of the highly gregarious Galápagos sea lion (Zalophus wollebaeki), we find several genetic clusters that correspond to spatially determined 'network communities'. Overall relatedness was low, and genetic structure in the network can be interpreted as an emergent property of philopatry and seems not to be primarily driven by targeted interactions among highly related individuals in family groups. Nevertheless, social relationships between directly adjacent individuals in the network were stronger among genetically more similar individuals. Taken together, these results suggest that even small differences in the degree of relatedness can influence behavioural decisions. This raises the fascinating prospect that kin selection may also apply to low levels of relatedness within densely packed animal groups where less obvious co-operative interactions such as increased tolerance and stress reduction are important.

Vocal mother-offspring communication in guinea pigs: females adjust maternal responsiveness to litter size.

BACKGROUND: In parent-offspring communication, vocal signals are often used to attract attention and offspring might call to induce parental behaviour. In guinea pigs (Cavia aperea f. porcellus) mothers wean larger litters later than small ones, but it is unknown whether this difference depends on processes induced during pregnancy or is influenced post-natally by the number of pups present. We here tested with playback-experiments using pup separation calls whether mothers with cross-fostered large experimental litters (four-pup-litters) were more responsive to offspring calls and maintained responsiveness for longer than mothers with small experimental litters (two-pup-litters). Mothers were tested when two pups were suckling i.e. when both teats were occupied. RESULTS: Mothers of four-pup litters responded stronger to broadcast pup separation calls than those with two-pup litters. Additionally, we tested the mothers' responsiveness to pup separation calls in the absence of their pups on day 8 and 20 of lactation. Mothers of four-pup litters responded stronger and showed no decrease in responsiveness from day 8 to 20, whereas mothers of two-pup litters responded less and decreased responsiveness from day 8 to 20. Mothers of four-pup litters also weaned their pups 5 days later than those of two-pup litters. CONCLUSION: Measured by their response to pup calls and by time to weaning, guinea pig mothers adjust maternal responsiveness to litter size. This behaviour is likely to be an adaptive strategy in resource allocation during reproduction.

Galápagos and Californian sea lions are separate species: Genetic analysis of the genus Zalophus and its implications for conservation management.

BACKGROUND: Accurate formal taxonomic designations are thought to be of critical importance for the conservation of endangered taxa. The Galápagos sea lion (GSL), being appreciated as a key element of the Galápagos marine ecosystem, has lately been listed as 'vulnerable' by the IUCN. To date there is, however, hardly any scientific evidence, whether it constitutes a separate entity from its abundant Californian neighbour (CSL). In this paper, we delineate the taxonomic relationships within the genus Zalophus being comprised of the Galápagos sea lion, the Californian sea lion and the already extinct Japanese sea lion (JSL). RESULTS: Using a set of different phylogenetic reconstruction approaches, we find support for monophyly of all three taxa without evidence of reticulation events. Molecular clock estimates place time to common ancestry of the Galápagos sea lion and the Californian sea lion at about 2.3 +/- 0.5 mya. Genetic separation is further suggested by diagnostic SNPs in the mitochondrial and nuclear genome. Microsatellite markers confirm this trend, showing numerous private alleles at most of the 25 investigated loci. Microsatellite-based estimates of genetic differentiation between the Galápagos sea lion and the Californian sea lion indicate significant genetic differentiation. Gene diversity is 14% lower in the Galápagos sea lion than in the Californian sea lion, but there is no evidence for recent bottleneck events in the Galápagos sea lion. CONCLUSION: Based on molecular evidence we build a case for classifying the Galápagos sea lion (Zalophus wollebaeki), the Californian sea lion (Zalophus californianus) and the Japanese sea lion (Zalophus japonicus) as true species. As morphological characters do not necessarily fully reflect the rapid divergence on the molecular level, the study can be considered as a test case for deriving species status from molecular evidence. We further use the results to discuss the role of genetics in conservation policy for an organism that already is under the general protection of the habitat it lives in.