The reproductive advantages of a long life: longevity and senescence in wild female African elephants.

Long-lived species such as elephants, whales and primates exhibit extended post-fertile survival compared to species with shorter lifespans but data on age-related fecundity and survival are limited to few species or populations. We assess relationships between longevity, reproductive onset, reproductive rate and age for 834 longitudinally monitored wild female African elephants in Amboseli, Kenya. The mean known age at first reproduction was 13.8 years; only 5 % commenced reproduction by 10 years. Early reproducers (<12.5 years) had higher age-specific fertility rates than did females who commenced reproduction late (15+ years) with no differences in survival between these groups. Age-specific reproductive rates of females dying before 40 years were reduced by comparison to same-aged survivors, illustrating a mortality filter and reproductive advantages of a long life. Overall, 95 % of fertility was completed before 50, and 95 % of mortality experienced by age 65, with a mean life expectancy of 41 years for females who survived to the minimum age at first birth (9 years). Elephant females have a relatively long period (c. 16 years) of viability after 95 % completed fertility, although reproduction does not entirely cease until they are over 65. We found no evidence of increased investment among females aged over 40 in terms of delay to next birth or calf mortality. The presence of a mother reproducing simultaneously with her daughter was associated with higher rates of daughter reproduction suggesting advantages from maternal (and grandmaternal) co-residence during reproduction.

The influence of social structure, habitat, and host traits on the transmission of Escherichia coli in wild elephants.

Social structure is proposed to influence the transmission of both directly and environmentally transmitted infectious agents. However in natural populations, many other factors also influence transmission, including variation in individual susceptibility and aspects of the environment that promote or inhibit exposure to infection. We used a population genetic approach to investigate the effects of social structure, environment, and host traits on the transmission of Escherichia coli infecting two populations of wild elephants: one in Amboseli National Park and another in Samburu National Reserve, Kenya. If E. coli transmission is strongly influenced by elephant social structure, E. coli infecting elephants from the same social group should be genetically more similar than E. coli sampled from members of different social groups. However, we found no support for this prediction. Instead, E. coli was panmictic across social groups, and transmission patterns were largely dominated by habitat and host traits. For instance, habitat overlap between elephant social groups predicted E. coli genetic similarity, but only in the relatively drier habitat of Samburu, and not in Amboseli, where the habitat contains large, permanent swamps. In terms of host traits, adult males were infected with more diverse haplotypes, and males were slightly more likely to harbor strains with higher pathogenic potential, as compared to adult females. In addition, elephants from similar birth cohorts were infected with genetically more similar E. coli than elephants more disparate in age. This age-structured transmission may be driven by temporal shifts in genetic structure of E. coli in the environment and the effects of age on bacterial colonization. Together, our results support the idea that, in elephants, social structure often will not exhibit strong effects on the transmission of generalist, fecal-oral transmitted bacteria. We discuss our results in the context of social, environmental, and host-related factors that influence transmission patterns.

Enduring consequences of early experiences: 40 year effects on survival and success among African elephants (Loxodonta africana).

Growth from conception to reproductive onset in African elephants (Loxodonta africana) provides insights into phenotypic plasticity, individual adaptive plastic responses and facultative maternal investment. Using growth for 867 and life histories for 2652 elephants over 40 years, we demonstrate that maternal inexperience plus drought in early life result in reduced growth rates for sons and higher mortality for both sexes. Slow growth during early lactation was associated with smaller adult size, later age at first reproduction, reduced lifetime survival and consequently limited reproductive output. These enduring effects of trading slow early growth against immediate survival were apparent over the very long term; delayed downstream consequences were unexpected for a species with a maximum longevity of 70+ years and unpredictable environmental experiences.

Wild female African elephants (Loxodonta africana) exhibit personality traits of leadership and social integration.

Animal personalities have been demonstrated for almost 200 species, with stable dimensions of responses (aggressive to fearful; shy to bold) across contexts and with a heritable basis to these traits. As a long-lived and highly social species, elephants (Loxodonta africana) were expected to demonstrate complex dimensions to individual characteristics or personalities, which would be obvious to human observers and validated by behavioral observations. We used principal-components analysis of ratings on 26 behavioral adjectives applied to one social unit, coded as the EB family, which has been observed for 38 years. Eleven adult females were rated by four observers and found to have individually variable traits on four dimensions described by principal-components analysis. The first component was associated with effective and confident family leadership. Component 2 was age-related, and defined by playfulness, exploration and high levels of activity, suggesting both an experience and an age-related element to its structure. Component 3 represented gentleness and at its other extreme, aggression, and Component 4 was related to constancy (predictability and popularity), with both of these latter components reflecting social integration. Leadership among elephant females represents the successful negotiation among individual interests, and our components were related to a capacity to affect the behavior of others in the absence of aggressive dominance. The family matriarch, Echo, was high on elements associated with leadership. The importance of the matriarch in this family's success suggests that elements of personality may underlie interfamilial variation in long-term survival and reproduction.

The influence of life history milestones and association networks on crop-raiding behavior in male African elephants.

Factors that influence learning and the spread of behavior in wild animal populations are important for understanding species responses to changing environments and for species conservation. In populations of wildlife species that come into conflict with humans by raiding cultivated crops, simple models of exposure of individual animals to crops do not entirely explain the prevalence of crop raiding behavior. We investigated the influence of life history milestones using age and association patterns on the probability of being a crop raider among wild free ranging male African elephants; we focused on males because female elephants are not known to raid crops in our study population. We examined several features of an elephant association network; network density, community structure and association based on age similarity since they are known to influence the spread of behaviors in a population. We found that older males were more likely to be raiders than younger males, that males were more likely to be raiders when their closest associates were also raiders, and that males were more likely to be raiders when their second closest associates were raiders older than them. The male association network had sparse associations, a tendency for individuals similar in age and raiding status to associate, and a strong community structure. However, raiders were randomly distributed between communities. These features of the elephant association network may limit the spread of raiding behavior and likely determine the prevalence of raiding behavior in elephant populations. Our results suggest that social learning has a major influence on the acquisition of raiding behavior in younger males whereas life history factors are important drivers of raiding behavior in older males. Further, both life-history and network patterns may influence the acquisition and spread of complex behaviors in animal populations and provide insight on managing human-wildlife conflict.

Age determination by back length for African savanna elephants: extending age assessment techniques for aerial-based surveys.

Determining the age of individuals in a population can lead to a better understanding of population dynamics through age structure analysis and estimation of age-specific fecundity and survival rates. Shoulder height has been used to accurately assign age to free-ranging African savanna elephants. However, back length may provide an analog measurable in aerial-based surveys. We assessed the relationship between back length and age for known-age elephants in Amboseli National Park, Kenya, and Addo Elephant National Park, South Africa. We also compared age- and sex-specific back lengths between these populations and compared adult female back lengths across 11 widely dispersed populations in five African countries. Sex-specific Von Bertalanffy growth curves provided a good fit to the back length data of known-age individuals. Based on back length, accurate ages could be assigned relatively precisely for females up to 23 years of age and males up to 17. The female back length curve allowed more precise age assignment to older females than the curve for shoulder height does, probably because of divergence between the respective growth curves. However, this did not appear to be the case for males, but the sample of known-age males was limited to ≤27 years. Age- and sex-specific back lengths were similar in Amboseli National Park and Addo Elephant National Park. Furthermore, while adult female back lengths in the three Zambian populations were generally shorter than in other populations, back lengths in the remaining eight populations did not differ significantly, in support of claims that growth patterns of African savanna elephants are similar over wide geographic regions. Thus, the growth curves presented here should allow researchers to use aerial-based surveys to assign ages to elephants with greater precision than previously possible and, therefore, to estimate population variables.

Why do African elephants (Loxodonta africana) simulate oestrus? An analysis of longitudinal data.

Female African elephants signal oestrus via chemicals in their urine, but they also exhibit characteristic changes to their posture, gait and behaviour when sexually receptive. Free-ranging females visually signal receptivity by holding their heads and tails high, walking with an exaggerated gait, and displaying increased tactile behaviour towards males. Parous females occasionally exhibit these visual signals at times when they are thought not to be cycling and without attracting interest from musth males. Using demographic and behavioural records spanning a continuous 28-year period, we investigated the occurrence of this "simulated" oestrus behaviour. We show that parous females in the Amboseli elephant population do simulate receptive oestrus behaviours, and this false oestrus occurs disproportionately in the presence of naïve female kin who are observed coming into oestrus for the first time. We compare several alternative hypotheses for the occurrence of this simulation: 1) false oestrus has no functional purpose (e.g., it merely results from abnormal hormonal changes); 2) false oestrus increases the reproductive success of the simulating female, by inducing sexual receptivity; and 3) false oestrus increases the inclusive fitness of the simulating female, either by increasing the access of related females to suitable males, or by encouraging appropriate oestrus behaviours from female relatives who are not responding correctly to males. Although the observed data do not fully conform to the predictions of any of these hypotheses, we rule out the first two, and tentatively suggest that parous females most likely exhibit false oestrus behaviours in order to demonstrate to naïve relatives at whom to direct their behaviour.

Major histocompatibility complex variation and evolution at a single, expressed DQA locus in two genera of elephants.

Genes of the vertebrate major histocompatibility complex (MHC) are crucial to defense against infectious disease, provide an important measure of functional genetic diversity, and have been implicated in mate choice and kin recognition. As a result, MHC loci have been characterized for a number of vertebrate species, especially mammals;however, elephants are a notable exception. Our study is the first to characterize patterns of genetic diversity and natural selection in the elephant MHC. We did so using DNA sequences from a single, expressed DQA locus in elephants.We characterized six alleles in 30 African elephants(Loxodonta africana) and four alleles in three Asian elephants (Elephas maximus). In addition, for two of the African alleles and three of the Asian alleles, we characterized complete coding sequences (exons 1-5) and nearly complete non-coding sequences (introns 2-4) for the class II DQA loci. Compared to DQA in other wild mammals, we found moderate polymorphism and allelic diversity and similar patterns of selection; patterns of non-synonymous and synonymous substitutions were consistent with balancing selection acting on the peptides involved in antigen binding in the second exon. In addition, balancing selection has led to strong trans-species allelism that has maintained multiple allelic lineages across both genera of extant elephants for at least 6 million years. We discuss our results in the context of MHC diversity in other mammals and patterns of evolution in elephants.

Fine-scale population genetic structure in a fission-fusion society.

Nonrandom patterns of mating and dispersal create fine-scale genetic structure in natural populations - especially of social mammals - with important evolutionary and conservation genetic consequences. Such structure is well-characterized for typical mammalian societies; that is, societies where social group composition is stable, dispersal is male-biased, and males form permanent breeding associations in just one or a few social groups over the course of their lives. However, genetic structure is not well understood for social mammals that differ from this pattern, including elephants. In elephant societies, social groups fission and fuse, and males never form permanent breeding associations with female groups. Here, we combine 33 years of behavioural observations with genetic information for 545 African elephants (Loxodonta africana), to investigate how mating and dispersal behaviours structure genetic variation between social groups and across age classes. We found that, like most social mammals, female matrilocality in elephants creates co-ancestry within core social groups and significant genetic differentiation between groups (Phi(ST) = 0.058). However, unlike typical social mammals, male elephants do not bias reproduction towards a limited subset of social groups, and instead breed randomly across the population. As a result, reproductively dominant males mediate gene flow between core groups, which creates cohorts of similar-aged paternal relatives across the population. Because poaching tends to eliminate the oldest elephants from populations, illegal hunting and poaching are likely to erode fine-scale genetic structure. We discuss our results and their evolutionary and conservation genetic implications in the context of other social mammals.

African elephants have expectations about the locations of out-of-sight family members.

Monitoring the location of conspecifics may be important to social mammals. Here, we use an expectancy-violation paradigm to test the ability of African elephants (Loxodonta africana) to keep track of their social companions from olfactory cues. We presented elephants with samples of earth mixed with urine from female conspecifics that were either kin or unrelated to them, and either unexpected or highly predictable at that location. From behavioural measurements of the elephants' reactions, we show that African elephants can recognize up to 17 females and possibly up to 30 family members from cues present in the urine-earth mix, and that they keep track of the location of these individuals in relation to themselves.

Elephants classify human ethnic groups by odor and garment color.

Animals can benefit from classifying predators or other dangers into categories, tailoring their escape strategies to the type and nature of the risk. Studies of alarm vocalizations have revealed various levels of sophistication in classification. In many taxa, reactions to danger are inflexible, but some species can learn the level of threat presented by the local population of a predator or by specific, recognizable individuals. Some species distinguish several species of predator, giving differentiated warning calls and escape reactions; here, we explore an animal's classification of subgroups within a species. We show that elephants distinguish at least two Kenyan ethnic groups and can identify them by olfactory and color cues independently. In the Amboseli ecosystem, Kenya, young Maasai men demonstrate virility by spearing elephants (Loxodonta africana), but Kamba agriculturalists pose little threat. Elephants showed greater fear when they detected the scent of garments previously worn by Maasai than by Kamba men, and they reacted aggressively to the color associated with Maasai. Elephants are therefore able to classify members of a single species into subgroups that pose different degrees of danger.

Behavioural inbreeding avoidance in wild African elephants.

The costs of inbreeding depression, as well as the opportunity costs of inbreeding avoidance, determine whether and which mechanisms of inbreeding avoidance evolve. In African elephants, sex-biased dispersal does not lead to the complete separation of male and female relatives, and so individuals may experience selection to recognize kin and avoid inbreeding. However, because estrous females are rare and male-male competition for mates is intense, the opportunity costs of inbreeding avoidance may be high, particularly for males. Here we combine 28 years of behavioural and demographic data on wild elephants with genotypes from 545 adult females, adult males, and calves in Amboseli National Park, Kenya, to test the hypothesis that elephants engage in sexual behaviour and reproduction with relatives less often than expected by chance. We found support for this hypothesis: males engaged in proportionally fewer sexual behaviours and sired proportionally fewer offspring with females that were natal family members or close genetic relatives (both maternal and paternal) than they did with nonkin. We discuss the relevance of these results for understanding the evolution of inbreeding avoidance and for elephant conservation.

The ties that bind: genetic relatedness predicts the fission and fusion of social groups in wild African elephants.

Many social animals live in stable groups. In contrast, African savannah elephants (Loxodonta africana) live in unusually fluid, fission-fusion societies. That is, 'core' social groups are composed of predictable sets of individuals; however, over the course of hours or days, these groups may temporarily divide and reunite, or they may fuse with other social groups to form much larger social units. Here, we test the hypothesis that genetic relatedness predicts patterns of group fission and fusion among wild, female African elephants. Our study of a single Kenyan population spans 236 individuals in 45 core social groups, genotyped at 11 microsatellite and one mitochondrial DNA (mtDNA) locus. We found that genetic relatedness predicted group fission; adult females remained with their first order maternal relatives when core groups fissioned temporarily. Relatedness also predicted temporary fusion between social groups; core groups were more likely to fuse with each other when the oldest females in each group were genetic relatives. Groups that shared mtDNA haplotypes were also significantly more likely to fuse than groups that did not share mtDNA. Our results suggest that associations between core social groups persist for decades after the original maternal kin have died. We discuss these results in the context of kin selection and its possible role in the evolution of elephant sociality.