Heterogeneity in male horn growth and longevity in a highly sexually dimorphic ungulate

In sexually dimorphic ungulates, sexual selection favoring rapid horn growth in males may be counterbalanced by a decrease in longevity if horns are costly to produce and maintain. Alternatively, if early horn growth varied with individual quality, it may be positively correlated with longevity. We studied Alpine ibex Capra ibex in the Gran Paradiso National Park, Italy, to test these alternatives by comparing early horn growth and longevity of 383 males that died from natural causes. After accounting for age at death, total horn length after age 5 was positively correlated with horn growth from two to four years. Individuals with the fastest horn growth as young adults also had the longest horns later in life. Annual horn growth increments between two and six years of age were independent of longevity for ibex whose age at death ranged from 8 to 16 years. Our results suggest that growing long horns does not constrain longevity. Of the variability in horn length, 22% could be explained by individual heterogeneity, suggesting persistent differences in phenotypic quality among males. Research on unhunted populations of sexually dimorphic ungulates documents how natural mortality varies according to horn or antler size, and can help reduce the impact of sport hunting on natural processes.     

Alpine ibex males grow large horns at no survival cost for most of their lifetime

Large horns or antlers require a high energy allocation to produce and carry both physiological and social reproductive costs. Following the principle of energy allocation that implies trade-offs among fitness components, growing large weapons early in life should thus reduce future growth and survival. Evidence for such costs is ambiguous, however, partly because individual heterogeneity can counterbalance trade-offs. Individuals with larger horns or antlers may be of better quality and thus have a greater capacity to survive. We investigated trade-offs between male early horn growth and future horn growth, baseline mortality, onset of actuarial senescence, and rate of ageing in an Alpine ibex (Capra ibex ibex) population. Horn growth of males in early life was positively correlated to their horn length throughout their entire life. Cohort variation and individual heterogeneity both accounted for among-individual variation in horn length, suggesting both long-lasting effects of early life conditions and individual-specific horn growth trajectories. Early horn growth did not influence annual survival until 12 years of age, indicating that males do not invest in horn growth at survival costs over most of their lifetime. However, males with fast-growing horns early in life tended to have lower survival at very old ages. Individual heterogeneity, along with the particular life-history tactic of male ibex (weak participation to the rut until an old age after which they burn out in high mating investment), are likely to explain why the expected trade-off between horn growth and survival does not show up, at least until very old ages.     

Age-dependent genetic effects on a secondary sexual trait in male Alpine ibex, Capra ibex

Secondary sexual traits, such as horns in ungulates, may be good indicators of genetic quality because they are costly to develop. Genetic effects on such traits may be revealed by examining correlations between multilocus heterozygosity (MLH) and trait value. Correlations between MLH and fitness traits, termed heterozygosity-fitness correlations (HFC), may reflect inbreeding depression or associative overdominance of neutral microsatellite loci with loci directly affecting fitness traits. We investigated HFCs for horn growth, body mass and faecal counts of nematode eggs in wild Alpine ibex (Capra ibex). We also tested if individual inbreeding coefficients (f') estimated from microsatellite data were more strongly correlated with fitness traits than MLH. MLH was more strongly associated with trait variation than f'. We found HFC for horn growth but not for body mass or faecal counts of nematode eggs. The effect of MLH on horn growth was age-specific. The slope of the correlation between MLH and yearly horn growth changed from negative to positive as males aged, in accordance with the mutation accumulation theory of the evolution of senescence. Our results suggest that the horns of ibex males are an honest signal of genetic quality.     

Compensatory Growth Limits Opportunities for Artificial Selection in Alpine Chamois

ABSTRACT In ungulates, big males with large weapons typically outcompete other males over access to estrous females. In many species, rapid early growth leads to large adult mass and weapon size. We compared males in one hunted and one protected population of Alpine chamois (Rupicapra rupicapra) to examine the relationship between horn length and body mass. We assessed whether early development and hunter selectivity affected age-specific patterns of body and horn size and whether sport hunting could be an artificial selection pressure favoring smaller horns. Adult horn length was mostly independent of body mass. For adult males, the coefficient of variation of horn length (0.06) was <50% of that for body mass (0.16), suggesting that horn length presents a lower potential for selection and may be less important for male mating success than is body mass. Surprisingly, early development did not affect adult mass because of apparent compensatory growth. We found few differences in body and horn size between hunted and protected populations, suggesting the absence of strong effects of hunting on male phenotype. If horn length has a limited role in male reproductive success, hunter selectivity for males with longer horns is unlikely to lead to an artificial selective pressure on horn size. These results imply that the potential evolutionary effects of selective hunting depend on how the characteristics selected by hunters affect individual reproductive success.     

Habitat and Harvesting Practices Influence Horn Growth of Male Ibex

Size-selective harvesting of wild ungulates can trigger a range of ecological and evolutionary consequences. It remains unclear how environmental conditions, including changes in habitat, climate, and local weather conditions, dilute or strengthen the effects of trophy hunting. We analyzed horn length measurements of 2,815 male ibex (Capra pyrenaica) that were harvested from 1995 to 2017 in Els Ports de Tortosa i Beseit National Hunting Reserve in northeastern Spain. We used linear mixed models to determine the magnitude of inter-individual horn growth variability and partial least square path models to evaluate long-term effects of environmental change, population size, and hunting strategy on horn growth. Age-specific horn length significantly decreased over the study period, and nearly a quarter (23%) of its annual variation was attributed to individual heterogeneity among males. The encroachment of pine (Pinus spp.) forests had a negative effect on annual horn growth, possibly through nutritional impoverishment. The harvesting of trophy and selective individuals (e.g., small-horned males) from the entire population increased horn growth, probably because it reduced the competition for resources and prevented breeding of these smaller males. Local weather conditions and population size did not influence horn growth. Our study demonstrates how habitat changes are altering the horn growth of male ibex. We suggest that habitat interventions, such the thinning of pine forests, can contribute to securing the sustainability of trophy hunting. Even in situations where size-selective harvesting is not causing a detectable phenotypic response, management actions leading to the expansion of preferred land cover types, such as grass-rich open areas, can have a positive effect on ungulate fitness. Forest encroachment on open meadows and heterogeneous grasslands is pervasive throughout Mediterranean ecosystems. Therefore, our management recommendations can be extended to the landscape level, which will have the potential to mitigate the side effects of habitat deterioration on the phenotypic traits of wild ibex. © 2020 The Wildlife Society.     

European springtime temperature synchronises ibex horn growth across the eastern Swiss Alps

Direct effects of climate change on animal physiology, and indirect impacts from disruption of seasonal synchrony and breakdown of trophic interactions are particularly severe in Arctic and Alpine ecosystems. Unravelling biotic from abiotic drivers, however, remains challenging because high‐resolution animal population data are often limited in space and time. Here, we show that variation in annual horn growth (an indirect proxy for individual performance) of 8043 male Alpine ibex (Capra ibex) over the past four decades is well synchronised among eight disjunct colonies in the eastern Swiss Alps. Elevated March to May temperatures, causing premature melting of Alpine snowcover, earlier plant phenology and subsequent improvement of ibex food resources, fuelled annual horn growth. These results reveal dependency of local trophic interactions on large‐scale climate dynamics, and provide evidence that declining herbivore performance is not a universal response to global warming even for high‐altitude populations that are also harvested.     

The role of phenotypic plasticity in responses of hunted thinhorn sheep ram horn growth to changing climate conditions

When phenotypic change occurs over time in wildlife populations, it can be difficult to determine to what degree it is because of genetic effects or phenotypic plasticity. Here, we assess phenotypic changes over time in horn length and volume of thinhorn sheep (Ovis dalli) rams from Yukon Territory, Canada. We considered 42 years of horn growth from over 50 000 growth measurements in over 8000 individuals. We found that weather explained a large proportion of the annual fluctuation in horn growth, being particularly sensitive to spring weather. Only 2.5% of variance in horn length growth could be explained by an individual effect, and thus any genetic changes over the time period could only have had a small effect on phenotypes. Our findings allow insight into the capacity for horn morphology to react to selection pressures and demonstrate the overall importance of climate in determining growth.     

Is there a trade‐off between horn growth and survival in adult female chamois?

Life‐history theory predicts trade‐offs in energy allocation between different life‐history traits when resources are limited, i.e. certain traits should be negatively correlated. However, individuals differ in their ability to acquire resources, which can lead to positive correlations between traits at the population level. Here, we investigated the consequences of the allocation in horn growth and body mass on survival in a bovid (Rupicapra rupicapra) with capture‐mark re‐sighting data on 161 females. In female ungulates, body mass often covaries positively with demographic performance and the few studies on horn size suggest that this trait could be a signal of individual quality. Thus, we expected to measure positive correlations between the allocation in these traits and female survival. However, body mass was not correlated to female survival and there was only a negative, though marginal, effect of horn growth. Hence, it seems that the allocation in growth is not an indicator of female quality. Future studies could investigate the importance of growth on female reproduction to evaluate its effect on lifetime reproductive success. Moreover, it is important to confirm in other populations our result that suggests a cost of the allocation in horn growth to better understand the presence of horns in female bovids. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 516–521.     

Horn growth related to testosterone secretion in two wild Mediterranean ruminant species: the Spanish ibex (Capra pyrenaica hispanica) and European mouflon (Ovis orientalis musimon)

Seasonal variations in the horn development and testicular activity of the Spanish ibex (Capra pyrenaica hispanica) (n=6) and European mouflon (Ovis orientalis musimon) (n=5) were monitored to determine the role of increasing testosterone concentration on the arrest of horn growth during the rutting season. Marked seasonal variations in the rate of horn growth (P<0.01) and testicular activity (P<0.001) were seen in both species, although the magnitude and timing of these changes were different (P<0.01). Horn growth rate was inversely correlated to seasonal levels in testosterone plasma concentration in both species (ibex: R=-0.45, P<0.01; mouflon R=-0.51, P<0.01). In the mouflon, the increase in plasma testosterone concentration recorded in September (P<0.05 compared with the lowest concentration) coincided with a significant reduction in horn growth (P<0.05). In the ibex, the increase in plasma testosterone concentration in October (P<0.05 compared with the lowest concentration) was associated with a significant arrest of horn growth in November (P<0.05). These results appear to support the hypothesis that high peripheral plasma levels of testosterone are linked with the seasonal arrest of horn growth during the rutting period.     

ARTIFICIAL SELECTION ON HORN LENGTH-BODY SIZE ALLOMETRY IN THE HORNED BEETLE ONTHOPHAGUS ACUMINATUS (COLEOPTERA: SCARABAEIDAE)

Males of the horned beetle Onthophagus acuminatus Har. (Coleoptera: Scarabaeidae) exhibit horn length dimorphism due to a sigmoidal allometric relationship between horn length and body size: the steep slope of the allometry around the inflection of the sigmoid curve separates males into two groups; those larger than this inflection possess long horns, and those smaller than this inflection have short horns or lack horns. I examined the genetic basis of the allometric relationship between horn length and body size by selecting males that produced unusually long horns, and males that produced unusually short horns, for their respective body sizes. After seven generations of selection, lines selected for relatively long horns had significantly longer horn lengths for a given body size than lines selected for relatively short horns, indicating a heritable component to variation in the allometry. The sigmoidal shape of the allometry was not affected by this selection regime. Rather, selected lines differed in the position of the allometry along the body size axis. One consequence of lateral shifts in this allometric relationship was that the body size separating horned from hornless males (the point of inflection of the sigmoid curve) differed between selection lines: lines in which males were selected for relatively long horns began horn production at smaller body sizes than lines selected for relatively short horns. These results suggest that populations can evolve in response to selection on male horn length through modification of the growth relationship between horn length and body size.     

Linear and threshold-dependent expression of secondary sexual traits in the same individual: insights from a horned beetle (Coleoptera: Scarabaeidae)

Elaborate horns or horn‐like structures in male scarab beetles commonly scale with body size either (a) in a linear fashion with horn size increasing relatively faster than body size or (b) in a threshold‐dependent, sigmoid fashion; that is, males smaller than a certain critical body size develop no or only rudimentary horns, whereas males larger than the threshold size express fully developed horns. The development of linear vs. sigmoid scaling relationships is thought to require fundamentally different regulatory mechanisms. Here we show that such disparate regulatory mechanisms may co‐occur in the same individual. Large males of the south‐east Asian Onthophagus (Proagoderus) watanabei (Ochi & Kon) (Scarabaeidae, Onthophagini) develop a pair of long, curved head horns as well as a single thoracic horn. We show that unlike paired head horns in a large number of Onthophagus species, in O. watanabei the relationship between head horns and body size is best explained by a linear model. Large males develop disproportionately longer horns than small males, but the difference in relative horn sizes across the range of body sizes is small compared to other Onthophagus species. However, the scaling relationship between the thoracic horn and body size is best explained by a strongly sigmoid model. Only males above a certain body size threshold express a thoracic horn and males smaller than this threshold express no horn at all. We found a significant positive correlation between head and thoracic horn length residuals, contrary to what would be expected if a resource allocation tradeoff during larval development would influence the length of both horn types. Our results suggest that the scaling relationship between body size and horn length, and the developmental regulation underlying these scaling relationships, may be quite different for different horns, even though these horns may develop in the same individual. We discuss our results in the context of the developmental biology of secondary sexual traits in beetles. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83 , 473–480.     

Long-distance photogrammetric trait estimation in free-ranging animals: A new approach

The acquisition of accurate information on the size of traits in animals is fundamental for the study of animal ecology and evolution and their management. We demonstrate how morphological traits of free-ranging animals can reliably be estimated on very large observation distances of several hundred meters by the use of ordinary digital photographic equipment and simple photogrammetric software. In our study, we estimated the length of horn annuli in free-ranging male Alpine ibex (Capra ibex) by taking already measured horn annuli of conspecifics on the same photographs as scaling units. Comparisons with hand-measured horn annuli lengths and repeatability analyses revealed a high accuracy of the photogrammetric estimates. If length estimations of specific horn annuli are based on multiple photographs measurement errors of <5.5 mm can be expected. In the current study the application of the described photogrammetric procedure increased the sample size of animals with known horn annuli length by an additional 104%. The presented photogrammetric procedure is of broad applicability and represents an easy, robust and cost-efficient method for the measuring of individuals in populations where animals are hard to capture or to approach.     

Direct and indirect causal effects of heterozygosity on fitness-related traits in Alpine ibex

Heterozygosity–fitness correlations (HFCs) are a useful tool to investigate the effects of inbreeding in wild populations, but are not informative in distinguishing between direct and indirect effects of heterozygosity on fitness-related traits. We tested HFCs in male Alpine ibex (Capra ibex) in a free-ranging population (which suffered a severe bottleneck at the end of the eighteenth century) and used confirmatory path analysis to disentangle the causal relationships between heterozygosity and fitness-related traits. We tested HFCs in 149 male individuals born between 1985 and 2009. We found that standardized multi-locus heterozygosity (MLH), calculated from 37 microsatellite loci, was related to body mass and horn growth, which are known to be important fitness-related traits, and to faecal egg counts (FECs) of nematode eggs, a proxy of parasite resistance. Then, using confirmatory path analysis, we were able to show that the effect of MLH on horn growth was not direct but mediated by body mass and FEC. HFCs do not necessarily imply direct genetic effects on fitness-related traits, which instead can be mediated by other traits in complex and unexpected ways.     

Morphological characteristics and ageing criteria of sand gazelle (<Emphasis Type="Italic">Gazella subgutturosa marica</Emphasis> Thomas, 1897) and their use for wildlife management

Data on some morphological characteristics of 165 male and 229 female sand gazelles (Gazella subgutturosa marica) collected during routine veterinary activity of a captive population at the King Khalid Wildlife Research Centre in central Saudi Arabia were examined for general baseline information on a little studied species. Measurements compared between the sexes and three age classes—juvenile, sub-adult and adult—included body mass, horn length (straight and curved), horn spread, neck circumference, shoulder height, forehead length, ear length and horn length (curved) to forehead and ear length ratios. All measurements were of known age individuals. The most valuable characteristics to use for age determination in the field are horn length (curved) and neck circumference for males and horn length (straight and/or curved) and shoulder height for females. The value of morphological characteristics correlated to known age animals for in situ management is discussed.     

Variation in the ontogenetic allometry of horn length in bovids along a body mass continuum

Allometric relationships describe the proportional covariation between morphological, physiological, or life‐history traits and the size of the organisms. Evolutionary allometries estimated among species are expected to result from species differences in ontogenetic allometry, but it remains uncertain whether ontogenetic allometric parameters and particularly the ontogenetic slope can evolve. In bovids, the nonlinear evolutionary allometry between horn length and body mass in males suggests systematic changes in ontogenetic allometry with increasing species body mass. To test this hypothesis, we estimated ontogenetic allometry between horn length and body mass in males and females of 19 bovid species ranging from ca. 5 to 700 kg. Ontogenetic allometry changed systematically with species body mass from steep ontogenetic allometries over a short period of horn growth in small species to shallow allometry with the growth period of horns matching the period of body mass increase in the largest species. Intermediate species displayed steep allometry over long period of horn growth. Females tended to display shallower ontogenetic allometry with longer horn growth compared to males, but these differences were weak and highly variable. These findings show that ontogenetic allometric slope evolved across species possibly as a response to size‐related changes in the selection pressures acting on horn length and body mass.     

Prolactin inhibition does not influence horn growth in two wild caprinae species: European mouflon (Ovis orientalis musimon) and Iberian ibex (Capra pyrenaica)

Studies on seasonal horn development and the endocrine mechanism regulating its pattern in wild ruminants are scarce. The aim of this paper was to study the influence of photoperiod and prolactin (PRL) on horn growth in two wild ruminant species: the European mouflon and the Iberian ibex. Eighteen male ibexes and 13 mouflon rams, maintained in captivity, were divided into three groups: a control group, kept under a natural photoperiod (latitude, 40°25′ N); a long-day group, exposed to an artificial photoperiod of 15-h light and 9-h darkness; and a group treated with bromocriptine (BCR; 10?mg twice weekly during spring and summer) to induce hypoprolactinaemia. Horn length growth (HLG) was recorded weekly for 18?months; plasma PRL concentrations were measured twice monthly by radioimmunoassay. In the ibexes of the long-day group, the period of strong horn development during spring–summer was significantly reduced by 2?months compared with the controls. In the mouflons of the long-day group, this same period was significantly increased by 9?months. In the BCR-treated animals, hypoprolactinaemia was observed in both species, but HLG was the same as in the corresponding controls. The present results suggest that the seasonal pattern of horn growth of wild ruminants is primarily modulated by photoperiod in a species-dependent manner. The persistence of resurgence of horn growth during spring in the BCR-induced hypoprolactinaemic animals of both species suggests that annual variations in blood PRL concentration have no effect on seasonal variation in horn growth.     

Allometric plasticity in a polyphenic beetle

Abstract 1. Environmental conditions, such as variation in nutrition, commonly contribute to morphological variation among individuals by affecting body size and the expression of certain morphological traits; however the scaling relationship between a morphological trait and body size over a range of body sizes is generally assumed not to change in response to environmental fluctuation (allometric plasticity), but instead to be constant and diagnostic for a particular trait and species or population. The work reported here examined diet‐induced allometric plasticity in the polyphenic beetle Onthophagus taurus Schreber (1759) (Coleoptera: Scarabaeidae). 2. Male O. taurus vary in body size depending on larval nutrition. Only males above a critical body size threshold express fully developed horns; males smaller than this threshold develop only rudimentary horns or no horns at all. 3. Field populations that naturally utilise two different resources for feeding larvae (horse dung vs. cow manure) exhibited significant differences in the average scaling relationship between body size and male horn length over the same range of body sizes. Males collected from cow manure populations expressed consistently longer horns for a given body size than males collected from horse dung populations. 4. Males reared in the laboratory on horse dung or cow manure also exhibited significant differences in the average scaling relationship between body size and horn length. Differences between laboratory populations reared on horse dung or cow manure were of the same kind and magnitude as differences between field populations that utilise these different resources naturally. 5. These findings suggest that between‐population differences in scaling relationships between horn length and body size can be the product of differences in the quality of resources available to developing larvae. Results are discussed in the context of onthophagine mating systems and recent insights in the developmental and endocrine control of horn polyphenisms.     

Seasonal variation in reproductive physiological status in the Iberian ibex (Capra pyrenaica) and its relationship with sperm freezability

The present work examines the relationship between seasonal changes in testicular function, accessory gland size, and horn growth in Iberian ibexes, as well as the relationship between these changes and the resistance of ibex spermatozoa to freezing-thawing. The size of the bulbourethral glands and seminal vesicles showed pronounced monthly variation (P < 0.001), which was correlated positively with the plasma testosterone concentration (P < 0.001) and scrotal circumference (P < 0.001). The size of the accessory sex glands peaked during the autumn. Overall, semen quality was markedly improved during autumn and winter. When horn growth was at a minimum during autumn and winter, semen quality and accessory gland size were all increased compared to in spring and summer. However, increased plasma testosterone levels in the autumn were strongly associated with reduced sperm freezability; thus, the cryosurvival of spermatozoa collected during the autumn was poorer than at other times of the year. In winter, however, when the plasma testosterone concentration fell to baseline, the negative effects of cryopreservation on the percentage of motile spermatozoa and on the integrity of the plasma membrane of frozen-thawed sperm cells were significantly less intense (P < 0.05). These findings show a clear relationship between the functional and morphological status of the different parts of the reproductive tract that optimises reproductive function during the breeding season in the ibex male. They also show that winter is the most suitable season for the collection and cryopreservation of ibex spermatozoa.     

Environmental and evolutionary effects on horn growth of male bighorn sheep

The development of male secondary sexual characters such as antlers or horns has substantial biological and socio‐economic importance because in many species these traits affect male fitness positively through sexual selection and negatively through trophy hunting. Both environmental conditions and selective hunting can affect horn growth but their relative importance remains unexplored. We first examined how a large‐scale climate index, the Pacific Decadal Oscillation (PDO), local weather and population density influenced both absolute and relative annual horn growth from birth to three years of male bighorn sheep Ovis canadensis over 42 years. We then examined the relative influence of environmental conditions and evolution mainly driven by trophy hunting on male horn length at three years of age. Horn growth was positively influenced by low population density and warm spring temperature, suggesting that ongoing climate change should lead to larger horns. Seasonal values of PDO were highly correlated. Horn growth increased with PDO in spring or summer at low density, but was weak at high density regardless of PDO. The interaction between population density and PDO in spring or summer accounted for a similar proportion of the observed annual variation in horn growth (32% or 37%) as did the additive effects of spring temperature and density (34%). When environmental conditions deteriorated, males allocated relatively more resources to summer mass gain than to horn growth, suggesting a conservative strategy favoring maintenance of condition over allocation to secondary sexual characters. Population density explained 27% of the variation in horn length, while evolutionary effects explained 9% of the variance. Thus, our study underlines the importance of both evolution and phenotypic plasticity on the development of a secondary sexual trait.     

Telomere attrition and growth: a life‐history framework and case study in common terns

The relationship between growth and age‐specific telomere length, as a proxy of somatic state, is increasingly investigated, but observed patterns vary and a predictive framework is lacking. We outline expectations based on the assumption that telomere maintenance is costly and argue that individual heterogeneity in resource acquisition is predicted to lead to positive covariance between growth and telomere length. However, canalization of resource allocation to the trait with a larger effect on fitness, rendering that trait relatively invariant, can cause the absence of covariance. In a case study of common tern (Sterna hirundo) chicks, in which hatching order is the main determinant of variation in resource acquisition within broods, we find that body mass, but not telomere length or attrition, varies with hatching order. Moreover, body mass and growth positively predict survival to fledging, whereas telomere length and attrition do not. Using a novel statistical method to quantify standardized variance in plasticity, we estimate between‐individual variation in telomere attrition to be only 12% of that of growth. Consistent with the relative invariance of telomere attrition, we find no correlation between age‐specific body mass or growth and telomere attrition. We suggest that common tern chicks prioritize investment in long‐term somatic state (as indicated by canalization of telomere maintenance) over immediate survival benefits of growth as part of an efficient brood reduction strategy that benefits the parents. As such, interspecific variation in the growth–telomere length relationship may be explained by the extent to which parents benefit from rapid mortality of excess offspring.