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Tusklessness in African Elephants a Future Trend

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  • CITES/MIKES

Abstract

In the South Luangwa National Park and the adjacent Lupande Game Management Area, located in Zambia's Eastern Province, the fraction of adult tuskless female elephants increased from 10·5% in 1969 to 38·2% in 1989, apparently as a direct result of selective illegal ivory hunting. From 1989 to 1993, the fraction of adult tuskless females declined from 38·2% to 28·70%, as a result of immigration of a relatively larger fraction of tusked females from adjacent Game Management Areas. Tusklessness appears to run in families and is sex-linked. Dans le Parc National de la Luangwa Sud et dans l'Aire de Gestion de la Faune de Lupande voisine, dans la province Orientale de Zambie, la proportion de femelles éléphants sans défenses est passée de 10,5% en 1969 à 38,2%, en 1989, suite directe semble-t-il de la chasse sélective pour l'ivoire. De 1989 à 1993, la proportion de femelles adultes sans défenses a baissé de 38,2%à 28,7%, en raison notamment de l'arrivée d'un assez grand nombre de femelles avec défenses en provenance des zones de gestion de la faune adjacentes, mais aussi à cause d'un changement de sex-ratio en faveur des mâles. L'absence de défences semble être un caractère familial et lié au sexe de l'animal.
... Given the evidence for heritability and femalespecificity of tusklessness in Gorongosa, we hypothesized that the phenotype is genetically inherited through a sex-linked locus (17,(19)(20)(21). We therefore searched for a pattern of inheritance that could explain the observed variation in tusk morphology. ...
... However, the exact genetic and developmental mechanisms leading to tusklessness and/or male nonviability remain unresolved. Although tuskless males do not occur in Gorongosa or in surveys of large sample sizes from Africa's most intensively studied elephant populations (17,21,36,37), there are anecdotal reports of tuskless males in several locations (20,38,39). We are unaware of any study that has firmly established a frequency of tuskless males beyond what could plausibly be explained by rare injuries or observer error (supplementary text and table S3), but we cannot rule out the possibility of alternative genetic mechanisms and/or genotype-environment interactions. ...
... We are unaware of any study that has firmly established a frequency of tuskless males beyond what could plausibly be explained by rare injuries or observer error (supplementary text and table S3), but we cannot rule out the possibility of alternative genetic mechanisms and/or genotype-environment interactions. Furthermore, intermediate single-tusked phenotypes commonly co-occur in family groups that also include bilaterally tuskless females (17,20,37). Although the evidence from Gorongosa is consistent with an X-linked dominant, male-lethal trait, continent-wide patterns of tusk expression and heritability may be the result of geographic variation in LD between AMELX and adjacent male-lethal loci, additional loci elsewhere in the species' genome, individual variation in patterns of X-chromosome inactivation, or some entirely different genetic mechanism. ...
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Understanding the evolutionary consequences of wildlife exploitation is increasingly important as harvesting becomes more efficient. We examined the impacts of ivory poaching during the Mozambican Civil War (1977 to 1992) on the evolution of African savanna elephants (Loxodonta africana) in Gorongosa National Park. Poaching resulted in strong selection that favored tusklessness amid a rapid population decline. Survey data revealed tusk-inheritance patterns consistent with an X chromosome–linked dominant, male-lethal trait. Whole-genome scans implicated two candidate genes with known roles in mammalian tooth development (AMELX and MEP1a), including the formation of enamel, dentin, cementum, and the periodontium. One of these loci (AMELX) is associated with an X-linked dominant, male-lethal syndrome in humans that diminishes the growth of maxillary lateral incisors (homologous to elephant tusks). This study provides evidence for rapid, poaching-mediated selection for the loss of a prominent anatomical trait in a keystone species.
... allelic richness, Canis lupus, genetic diversity, grey wolf, harvest, heterozygosity, relatedness In some cases, harvest can reduce genetic variation and create spatially based genetic structure in populations (Allendorf et al., 2008;Allendorf, Luikart, & Aitken, 2013). Harvest targeting large individuals can be strongly selective leading to reduced body size and earlier maturation rates in some populations (Jachmann, Berry, & Imae, 1995;Palkovacs, Moritsch, Contolini, & Pelletier, 2018;Swain, Sinclair, & Hanson, 2007;Therkildsen et al., 2019). Small populations can be particularly prone to negative genetic effects associated with harvest due to their small effective population size and inherently reduced genetic diversity overall (Allendorf et al., 2013). ...
... Naturally occurring mutation in microsatellites can create new alleles even in the absence of animals moving between groups, but the mutation rate (1.1 × 10 −2 to 3.9 × 10 −3 ; Francisco, Langston, Mellersh, Neal, & Ostrander, 1996;Irion et al., 2003;Lingaas et al., 1997) is likely to be relatively low compared to the rate of influx of new alleles from immigration. Harvest may be selective for certain phenotypic traits, as has been documented in many harvested species (Haldane, 1942;Hengeveld & Festa-Bianchet, 2011;Jachmann et al., 1995), but it has also been suggested that harvest of large mammals is not always a force of strong directional selection (Mysterud, 2011 (Bangs & Fritts, 1996). We posit that wolves in north Idaho will exhibit similar genetic diversity measures to those in central Idaho within several more generations as wolves disperse into the area from nearby recovered populations in Montana and British Columbia. ...
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Harvest can affect vital rates such as reproduction and survival, but also genetic measures of individual and population health. Gray wolves (Canis lupus ) live and breed in groups and effective population size is a small fraction of total abundance. As a result, genetic diversity of wolves may be particularly sensitive to harvest. We evaluated how harvest affected genetic diversity and relatedness in wolves. We hypothesized that harvest would 1) reduce relatedness of individuals within groups in a subpopulation but increase relatedness of individuals between groups due to increased local immigration, 2) increase individual heterozygosity and average allelic richness across groups in subpopulations and, 3) add new alleles to a subpopulation and decrease the number of private alleles in subpopulations due to an increase in breeding opportunities for unrelated individuals. We found harvest had no effect on observed heterozygosity of individuals or allelic richness at loci within subpopulations but was associated with a small, biologically insignificant effect on within‐group relatedness values in gray wolves. Harvest was, however, positively associated with increased relatedness of individuals between groups and a net gain (+16) of alleles into groups in subpopulations monitored since harvest began, although the number of private alleles in subpopulations overall declined. Harvest likely created opportunities for wolves to immigrate into nearby groups and breed, thereby making groups in subpopulations more related over time. Harvest appears to affect genetic diversity in wolves at the group and population level, but its effects are less apparent at the individual level given the population sizes we studied.
... Tusklessness in bush elephant females, a phenomenon rarely observed in the past, has continuously been increasing during the second half of the last century and at present time, especially in populations whose size decreased after severe poaching. Some consider the rapid increase in its frequency to be a phenotypic indicator of underlying genetic drift, a kind of human-driven natural selection, whereas others believe that selective hunting cannot provide adequate explanations, at least for some populations, considering tusklessness as a possible result of non-selective genetic changes in small-sized, isolated populations (see e.g Jachmann et al., 1995;Owens & Owens, 2009;Raubenheimer & Miniggio, 2016 for a discussion). ...
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The osteological collection of the Museo Civico di Zoologia of Rome (MCZR) counts 2 complete skeletons, 4 skulls with mandible, 4 skulls, 5 mandibles, 1 molariform tooth, and 11 more or less complete tusks of extant elephants. This research aims to identify to which elephant among those that lived in captivity and died at the Zoological Garden of Rome (ZGR) the cranial material belongs. The results of the qualitative and quantitative analysis, the inferred sex and age estimates permit to assert that the elephant cranial remains of MCZR's osteological collections belong to at least four taxa (Loxodonta africana, Loxodonta cyclotis, Elephas maximus maximus, and Elephas maximus sumatranus). 4 Asian and 3 African among the 14 Asian and the 6 African elephants that died at the ZGR from 1910 to 2012 were identified, while for 2 Asian elephants the identification was doubtful or highly uncertain. In addition, we acknowledged the presence of a large cranium of an African bush male of unknown provenance, a skull of an African forest male that lived at the Zoo of Naples from 1952 to 1955, and of a skull of a very young Asian elephant of unknown origin.
... Given these motivations, animals with particular traits or trait values (e.g., particular morph or size) are often targeted for harvesting, driving phenotypic change in harvested populations. Phenotypic responses to harvesting are well-documented in fishes, from freshwater recreational harvesting (Sutter et al., 2012) to marine commercial harvesting (Law, 2000), and in a wide variety of ungulates such as bighorn sheep (Pigeon et al., 2016) and elephants (Jachmann et al., 1995). More pervasively, selective harvest and associated phenotypic change is also documented in a variety of other mammalian and invertebrate taxa (Allendorf et al., 2008). ...
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Rapid evolution is ubiquitous in nature. We briefly review some of this quite broadly, particularly in the context of response to anthropogenic disturbances. Nowhere is this more evident, replicated and accessible to study than in cancer. Curiously cancer has been late - relative to fisheries, antibiotic resistance, pest management and evolution in human dominated landscapes - in recognizing the need for evolutionarily informed management strategies. The speed of evolution matters. Here, we employ game-theoretic modeling to compare time to progression with continuous maximum tolerable dose to that of adaptive therapy where treatment is discontinued when the population of cancer cells gets below half of its initial size and re-administered when the cancer cells recover, forming cycles with and without treatment. We show that the success of adaptive therapy relative to continuous maximum tolerable dose therapy is much higher if the population of cancer cells is defined by two cell types (sensitive vs. resistant in a polymorphic population). Additionally, the relative increase in time to progression increases with the speed of evolution. These results hold with and without a cost of resistance in cancer cells. On the other hand, treatment-induced resistance can be modeled as a quantitative trait in a monomorphic population of cancer cells. In that case, when evolution is rapid, there is no advantage to adaptive therapy. Initial responses to therapy are blunted by the cancer cells evolving too quickly. Our study emphasizes how cancer provides a unique system for studying rapid evolutionary changes within tumor ecosystems in response to human interventions; and allows us to contrast and compare this system to other human managed or dominated systems in nature.
... For instance, disproportionate targeting of wild animals for trophy features (e.g. horns, tusks, antlers) is known to cause rapid phenotypic responses in affected prey species, including higher rates of absence or reduction of trophy features (Jachmann et al., 1995;Sullivan et al., 2017). Directional pressure on a particular phenotype can also have pleiotropic effects on other phenotypes that are not the direct targets of selection (Sullivan et al., 2017). ...
Article
en The Indonesian island of Sulawesi harbours numerous early rock paintings of the endemic Sulawesi warty pig (Sus celebensis). Several S. celebensis images, including one dated to at least 45,500 years ago (ka), portray these suids with an anatomical character not observed in the living species: a pair of teat-like protuberances in the neck area. This feature seems to be most consistent morphologically with neck “wattles”, cutaneous appendages only manifested in modern domestic swine (Sus scrofa) and some other domesticated ungulates (e.g. goats). The notion that the trait portrayed by the Late Pleistocene artists is a domestication character is clearly contentious. We therefore consider: (1) whether we have misidentified the trait – a common problem in rock art analysis; (2) whether wattles are a genuine domestication trait; and (3) if so, whether the notion that Pleistocene people domesticated S. celebensis is plausible. A clear resolution to all of these problems evades us; however, our investigation of this anomaly in the ancient rock art poses important questions about the nature and complexity of early human–pig relations in this island. Résumé es L'ile Indonésienne de Sulawesi abrite de nombreuses anciennes peintures rupestres de son endémique cochon verruqueux (Sus celebensis). De nombreuses images de S. celebensis, y compris une datant d'au moins 45500 ans, décrivent ces suidés avec un caractère anatomique non observé chez les espèces contemporaines: une paire de protubérance mamellaire dans la zone du cou. Ce trait semble le plus proche morphologiquement des caroncules, appendices cutanés qui se manifestent seulement chez les porcs domestiques modernes (Sus scrofa) ainsi que chez d'autres ongulés domestiques (e.g. chèvres). Toutefois, la notion déclarant le trait décrit par les artistes du Pléistocène supérieur comme étant un caractère de domestication est clairement litigieuse. Nous considérons donc: (1) si nous avons identifiés à tort le trait – un problème commun dans l'analyse d'art rupestre; (2) si les caroncules peuvent être considérés comme de véritables traits de domestication; et (3) si tel est le cas, si la notion des peuples du Pléistocène domestiquant S. celebensis est plausible. Bien qu'une solution claire à tous ces problèmes nous échappe, notre investigation de cette anomalie dans l'art rupestre ancien posent d'importantes questions sur la nature et la complexité des premières relations homme-cochon sur cette ile.
... In long-lived mammals, hunting-induced selection commonly affects male secondary sexual traits, such as antlers, horns (Coltman et al., 2003;Jachmann et al., 1995;Pigeon et al., 2016), and body mass (Tenhumberg et al., 2004). However, hunting-induced selection on these traits is likely to have limited consequences for population dynamics of such species due to the weak correlation between body mass (or correlated secondary sexual traits value), and reproductive performance in mammals (Kuparinen & Festa-Bianchet, 2017), compared with fishes. ...
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Harvest, through its intensity and regulation, often results in selection on female reproductive traits. Changes in female traits can have demographic consequences, as they are fundamental in shaping population dynamics. It is thus imperative to understand and quantify the demographic consequences of changes in female reproductive traits to better understand and anticipate population trajectories under different harvest intensities and regulations. Here, using a dynamic, frequency‐dependent, population model of the intensively hunted brown bear (Ursus arctos) population in Sweden, we quantify and compare population responses to changes in four reproductive traits susceptible to harvest‐induced selection: litter size, weaning age, age at first reproduction, and annual probability to reproduce. We did so for different hunting quotas and under four possible hunting regulations: (i) no individuals are protected, (ii) mothers but not dependent offspring are protected, (iii) mothers and dependent offspring of the year (cubs) are protected, and (iv) entire family groups are protected (i.e., mothers and dependent offspring of any age). We found that population growth rate declines sharply with increasing hunting quotas. Increases in litter size and the probability to reproduce have the greatest potential to affect population growth rate. Population growth rate increases the most when mothers are protected. Adding protection on offspring (of any age), however, reduces the availability of bears for hunting, which feeds back to increase hunting pressure on the non‐protected categories of individuals, leading to reduced population growth. Finally, we found that changes in reproductive traits can dampen population declines at very high hunting quotas, but only when protecting mothers. Our results illustrate that changes in female reproductive traits may have context‐dependent consequences for demography. Thus, to predict population consequences of harvest‐induced selection in wild populations, it is critical to integrate both hunting intensity and regulation, especially if hunting selectivity targets female reproductive strategies.
... However, they also have evolutionary implications by, for example, selecting for smaller bodied individuals with smaller auxiliary structures or disrupting social structure (Coltman et al., 2003;Gobush, Mutayoba, & Wasser, 2008;Jachmann, Berry, & Imae, 1995). Recent evidence from regulated hunting in brown bears also suggests that hunting pressure may be responsible for shifts in reproductive strategies, life expectancy and reproductive value (Bischof et al., 2018). ...
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1. A changing environment directly influences birth and mortality rates, and thus population growth rates. However, population growth rates in the short‐term are also influenced by population age‐structure. Despite its importance, the contribution of age‐structure to population growth rates has rarely been explored empirically in wildlife populations with long‐term demographic data. 2. Here, we assessed how changes in age‐structure influenced short‐term population dynamics in a semi‐captive population of Asian elephants (Elephas maximus). 3. We addressed this question using a demographic dataset of female Asian elephants from timber camps in Myanmar spanning 45 years (1970‐2014). First, we explored temporal variation in age‐structure. Then, using annual matrix population models, we used a retrospective approach to assess the contributions of age‐structure and vital rates to short‐term population growth rates with respect to the average environment. 4. Age‐structure was highly variable over the study period, with large proportions of juveniles in the years 1970 and 1985, and made a substantial contribution to annual population growth rate deviations. High adult birth rates between 1970‐1980 would have resulted in large positive population growth rates, but these were prevented by a low proportion of reproductive‐aged females. 5. We highlight that an understanding of both age‐specific vital rates and age‐structure is needed to assess short‐term population dynamics. Furthermore, this example from a human‐managed system suggests that the importance of age‐structure may be accentuated in populations experiencing human disturbance where age‐structure is unstable, such as those in captivity or for endangered species. Ultimately, changes to the environment drive population dynamics by influencing birth and mortality rates, but understanding demographic structure is crucial for assessing population growth.
... While genomic approaches are useful for elephant conservation, the few elephant functional genomic studies currently available are limited to a small number of individuals and species [10][11][12][13] and the etiologies of many elephant traits with profound fitness (and therefore conservation-oriented) consequences have not yet been discovered. For instance, increased frequencies of tuskless elephants may be a response to selective pressures from ivory poaching [14][15][16] . The genes controlling tusk development, however, remain unknown. ...
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Disease susceptibility and defense are important factors in conservation, particularly for elephants. We report that in addition to endotheliotropic herpesvirus and tuberculosis, Asian elephants are also more susceptible to cancer than African elephants. To determine mechanisms underlying elephant traits including disease resistance, we analyzed genomic datasets from multiple individuals and species. We report a draft genome assembly for the Asian elephant and an improved African elephant assembly. We found 862 and 1,017 potential regulatory elements in Asian and African elephants, respectively, that are enriched near 5,034 differentially expressed genes in peripheral blood mononuclear cells between the two species. These genes are enriched in immunity pathways, including tumor-necrosis factor which plays a role in the elephant response to endotheliotropic herpesvirus. Some elephant TP53 retrogenes are being maintained by purifying selection and may contribute to cancer resistance in elephants. Positive selection scans revealed genes that may control tusk development, memory, and somatic maintenance. Our study provides an example of how genomics can inform functional immunological studies, which may improve conservation and medical care for elephants and translate into human therapies.
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In the process of avoiding predation, prey are faced with potentially fitness‐compromising trade‐offs that have implications for their survival and reproduction. The nature and strength of these non‐consumptive effects at the population level can be equivalent, or even greater, than consumptive effects. Many prey species have evolved defence mechanisms that are induced by predation risk. These inducible defences can be morphological or behavioural in nature. Extensive research has detected these defences in predator–prey communities across freshwater, marine and terrestrial ecosystems. Among this vast research however, an influential portion of these systems has not been widely considered. Humans inhabit a level in trophic systems above apex predators. In that position, humans have been referred to as a hyperkeystone or super predator species as they have shown a capacity to consume animals at rates many times higher than any other non‐human species. However, the extent to which humans induce adaptive defences in animals is not as clear. Systems involving large mammals may be particularly well‐suited for the study of human‐induced defences given that these species have been disproportionately exploited (for food and competition) over evolutionary time by humans. To begin this process we first had to examine the context in which large mammals could adaptively evolve inducible defences in relation to human lethality. With the plausibility of these conditions satisfied, we then conducted an extensive review to document the inducible defences that have been detected in large mammals. All of the 187 studies reviewed documented the behavioural plasticity of large mammals to human lethality. No morphological adaptive defences were detected. However, the extent to which the observed behavioural plasticity of large mammals is representative of adaptive inducible defences remains unclear because the fitness trade‐offs (i.e. costs), an integral condition for inducible defences to evolve, were implied rather than quantified among close to 92% of this research. We make recommendations for renewed ingenuity in the development of field experiments that can quantify these costs and discuss the implications of human lethality on the ecology, conservation and management of large mammals. A free Plain Language Summary can be found within the Supporting Information of this article. A free Plain Language Summary can be found within the Supporting Information of this article.
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Intra- and intersexual selection drives the evolution of secondary sexual traits, leading to increased body size, trait size and generally increased reproductive success in bearers with the largest, most attractive traits. Evolutionary change through natural selection is often thought of primarily in terms of genetic changes through mutations and adaptive selection. However, this view ignores the role of the plasticity in phenotypes and behaviour and its impact on accelerating or decelerating the expression of sexually selected traits. Here, we argue that sudden changes in selection pressures (e.g. predation pressure) may cause a cascade of behavioural responses, leading to a rapid change in the size of such traits. We propose that selective removal of individuals with the most prominent traits (such as large antlers or horns in male ungulates) induces behavioural changes in the surviving males, leading to a reduction in the growth of these traits (phenotypic expression). To test this idea, we used an individual-based simulation, parametrized with empirical data of male bighorn sheep, Ovis candensis. Our model shows that the expression (phenotype, not genotype) of the trait under selection (here horn size) can be negatively impacted, if the biggest, most dominant males in the population are removed. While the selective removal of prime males opens breeding opportunities for younger, smaller males, we predicted that it would come at the expense of growth and maintenance. As predicted, we observed a rapid decline in average male horn length in our model. We argue that this decline happens because smaller males, instead of allocating energy into growth, divert this energy towards participation in mating activities that are typically exclusively available to prime males. While our model deals with ecological life-history trade-offs, it cannot predict evolutionary outcomes. However, this nongenetic mechanism is important for the understanding of evolutionary processes because it describes how heritable traits can rapidly change because of behavioural plasticity, long before any genetic changes might be detectable.
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Bulls in musth leave their home range, travel far and fast, initiate more contacts with distant breeding herds, show aggression which overrides normal social male hierarchies, probably mate more frequently than non-musth bulls and then return to their home range. This behaviour is associated with elevated levels of serum testosterone and dihydrotestosterone. Elephants normally show a high degree of fidelity to sexually segregated adjoining home ranges, which results in regular contact between the same bulls and cows. This breeding strategy is applicable to older, dominant bulls within the locally resident hierarchy. The musth adaptation is a second strategy, whereby younger, lower ranking bulls (25-35 yr) can ensure more contacts with cows and maximize their chances of breeding. Because musth bulls mate far from their normal ranges the strategy promotes gene flow and ensures outbreeding. -from Author
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By using an elephant recognition file that was compiled during the study, data on group structures were obtained. A photogrammetric method was used to obtain data on the age-structure of the separate groups and the population as a whole. The age-structure is that of a young, healthy and rapidly increasing population. Peaks and troughs in the age-structure are related to local rainfall, which indirectly affects the conception-rate and age-specific mortality. The mean calving interval estimated by means of the photogrammetric device is 3.9 years, while the age of first conception can be as low as 7 years. A sex specific difference in the survival rate acts in favour of the female. In mature elephants, human interference such as selective shooting by poachers and the crop control unit also promotes a departure from a sex ratio of unity. The influence of human interference on the reproductive output of the population is discussed. The mean annual mortality rate is estimated as 7.7% from the survival curve of the population. This figure is high compared with figures on this parameter from other populations, which is explained by human activity.
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The trend in the volume of African ivory coming onto the world market suggests that African elephant populations have declined progressively since at least 1950 and that the rate of decline is presently accelerating. The process is well-advanced in East Africa where few elephants are predicted to survive beyond 1995 outside high-security areas. A similar trend is deduced for Africa as a whole but lagged about 20 years behind that of East Africa.
The reproductive physiology of the African elephant (Loxodonta africana)
  • J Hanks