Testosterone and reproductive effort in male primates

Considerable evidence suggests that the steroid hormone testosterone mediates major life-history trade-offs in vertebrates, promoting mating effort at the expense of parenting effort or survival. Observations from a range of wild primates support the “Challenge Hypothesis,” which posits that variation in male testosterone is more closely associated with aggressive mating competition than with reproductive physiology. In both seasonally and non-seasonally breeding species, males increase testosterone production primarily when competing for fecund females. In species where males compete to maintain long-term access to females, testosterone increases when males are threatened with losing access to females, rather than during mating periods. And when male status is linked to mating success, and dependent on aggression, high-ranking males normally maintain higher testosterone levels than subordinates, particularly when dominance hierarchies are unstable. Trade-offs between parenting effort and mating effort appear to be weak in most primates, because direct investment in the form of infant transport and provisioning is rare. Instead, infant protection is the primary form of paternal investment in the order. Testosterone does not inhibit this form of investment, which relies on male aggression. Testosterone has a wide range of effects in primates that plausibly function to support male competitive behavior. These include psychological effects related to dominance striving, analgesic effects, and effects on the development and maintenance of the armaments and adornments that males employ in mating competition.     

Negative density-dependent emigration of males in an increasing red deer population

In species with polygynous mating systems, females are regarded as food-limited, while males are limited by access to mates. When local density increases, forage availability declines, while mate access for males may increase due to an increasingly female-biased sex ratio. Density dependence in emigration rates may consequently differ between sexes. Here, we investigate emigration using mark-recovery data from 468 young red deer Cervus elaphus marked in Snillfjord, Norway over a 20-year period when the population size has increased sixfold. We demonstrate a strong negative density-dependent emigration rate in males, while female emigration rates were lower and independent of density. Emigrating males leaving the natal range settled in areas with lower density than expected by chance. Dispersing males moved 42 per cent longer at high density in 1997 (37 km) than at low density in 1977 (26 km), possibly caused by increasing saturation of deer in areas surrounding the marking sites. Our study highlights that pattern of density dependence in dispersal rates may differ markedly between sexes in highly polygynous species. Contrasting patterns reported in small-scale studies are suggestive that spatial scale of density variation may affect the pattern of temporal density dependence in emigration rates and distances.     

Behavioural factors affecting male reproductive success in red deer (Cervus elaphus)

Variation in reproductive success among adult red deer stags was related to harem size, and the duration and timing of breeding access. All three factors were affected by dominance (fighting success) during the rut. The number of hinds using a stag's rutting area and the duration of individual rutting activity also affected breeding access. Dominance rank in bachelor herds, which may affect access to hinds conceiving after the rut, was correlated with rank in the preceding but not the following rut.     

Early life expenditure in sexual competition is associated with increased reproductive senescence in male red deer

The evolutionary theories of senescence predict that investment in reproduction in early life should come at the cost of reduced somatic maintenance, and thus earlier or more rapid senescence. There is now growing support for such trade-offs in wild vertebrates, but these exclusively come from females. Here, we test this prediction in male red deer (Cervus elaphus) using detailed longitudinal data collected over a 40-year field study. We show that males which had larger harems and thereby allocated more resources to reproduction during early adulthood experienced higher rates of senescence in both harem size and rut duration. Males that carried antlers with more points during early life did not show more pronounced declines in reproductive traits in later life. Overall, we demonstrate that sexual competition shapes male reproductive senescence in wild red deer populations and provide rare empirical support for the disposable soma theory of ageing in males of polygynous vertebrate species.     

Long-term density-dependent changes in habitat selection in red deer (Cervus elaphus)

Understanding how habitat selection changes with population density is a key concept in population regulation, community composition and managing impacts on biodiversity and ecosystem services. At low density, it is expected that individuals select habitats in terms of their preference, but as population density increases, the availability of resources per individual declines on preferred habitats, leading to competition which forces some individuals to exploit less preferred habitats. Using spatial information of Scottish red deer (Cervus elaphus) winter counts, carried out in 110 areas across Scotland between 1961 and 2004 (a total of 1,206,495 deer observations), we showed how winter habitat niche breadth in red deer has widened with increasing population density. Heather moorland and montane habitats were most and least preferred for deer, respectively. Increasing density favoured the selection of grassland, to the detriment of the selection of heather moorland. The selection of heather and grassland decreased when temperature increased, while the selection of montane and peatland habitats increased. These findings are important for understanding how habitat use, density and population are likely to be affected by weather, and allow us to predict habitat impacts by large mammal herbivory and climate.     

Effects of melatonin implants on reproductive seasonality of male red deer (Cervus elaphus)

Red deer stags were treated with melatonin implants in 2 experiments designed to examine the control of reproductive seasonality. In Exp. 1, stags (n = 24) were allocated to 4 treatment groups: 2 groups were treated with 3 implants per stag each month from 8 November to 5 February (EM) or 9 December to 5 February (LM), 1 untreated group of control stags remained with the melatonin-treated stags (CC) and the other untreated control group remained isolated (IC). Melatonin treatment advanced the seasonal changes in scrotal circumference, liveweight, antler state and coat type compared with control stags. The extent of advancement was greater in EM than LM stags. In EM and LM stags, size of testes regressed rapidly and antlers were cast shortly after melatonin implants became exhausted in March. This was followed by an additional antler cycle and reproductive development and decline from June to November. EM and LM stags became synchronized with control stags 14-15 months after melatonin treatment began. The extra cycle of seasonal changes was more pronounced in EM than in LM stags. In Exp. 2, stags (n = 30) were allocated to 6 treatment groups: 4 groups were treated with 3 implants per stag at monthly intervals for 6 months from 22 June (J), 4 August (A), 16 September (S) and 23 October (O), a further group of stags was treated in the same manner for 12 months from 22 June (Y), and the remaining group was untreated (C). Compared with control stags, testicular regression and antler casting was delayed in Groups J, A and Y. These events occurred at the same time as in control stags in Groups S and O. Subsequent reproductive development was advanced in Groups S and O and delayed in Groups J, A and Y. The results demonstrated that treatment with melatonin implants in November or December advanced reproductive development. However, when stags were treated with melatonin implants from June to August, reproductive development was delayed, indicating a change in response to melatonin treatment during the year. The change in response to melatonin treatment between late winter and early spring was interpreted as a resetting of an endogenous circannual rhythm caused by a photoperiodic cue responsible for initiating the final stages of reproductive regression.     

Age- and density-dependent population dynamics in static and variable environments

We consider a general model of a single-species population with age- and density-dependent per capita birth and death rates. In a static environment we show that if the per capita death rate is independent of age, then the local stability of any stationary state is guaranteed by the requirement that, in the region of the steady state, the density dependence of the birth rate should be negative and that of the death rate positive. In a variable environment we show that, provided the system is locally stable, small environmental fluctuations will give rise to small age structure and population fluctuations which are related to the driving environmental fluctuations by a simple “transfer function.” We illustrate our general theory by examining a model with a per capita death rate which is age and density independent and a per capita birth rate which is zero up to some threshold age a₀, adopts a finite density-dependent value up to a maximum age a_o + α, and is zero thereafter. We conclude from this model that resonance due specifically to single-species age-structure effects will only be of practical importance in populations whose members have a life cycle consisting of a long immature phase followed by a short burst of intense reproductive effort (α a_o).     

Age-specific feeding cessation in male red deer during rut

Tactics for resource-use involve both using stored reserves (capital breeding) and feeding while reproducing (income breeding). In polygynous ungulates, males often use an income breeding strategy when young and shift to a capital breeding tactic at prime age. Little is known regarding why prime-aged males stop or largely reduce eating during rut but still remain inactive for as much time as before rut. A detailed exploration of how rumen content correlates with age and date may shed light on the ultimate causes of why some males stop eating. We provide quantitative empirical data on rumen content from red deer Cervus elaphus during the rutting season in Norway. In male red deer, rumen content declined with age, up to around 6 years of age. Above this age, rumen content was low and stable. A time-of-year effect on rumen content was best described with a second-order polynomial term, as rumen fill was lowest during mid-October when the mass loss of males and the ovulation rate of females both peak. We present two new hypotheses related to why males reduce eating ( physical rest and parasite hypotheses). Two related patterns need to be explained and better documented: (1) why are resting times stable before, after and during rut, and (2) why do non-prime-aged males eat more between rutting activities?     

Genetic and behavioural estimates of reproductive skew in male fallow deer

Populations of fallow deer, in general, have low genetic diversity. Nevertheless, we screened 39 microsatellite loci and identified 20 that were polymorphic and suitable to determine paternity of fallow deer. To date, paternity has been studied for 87, 110 and 152 fallow deer fawns born between 2000 and 2002. Our results confirm the existence of a strong polygynous mating system in our population and confirm that the number of copulations performed by males is globally a good estimator of their reproductive success: males which performed the largest proportion of matings fathered the largest proportion of fawns. Nevertheless, we report some differences between the two measurements of the males' reproductive success: measures of copulatory success underestimated the variance of the males' reproductive success. On average, males whose copulatory score exceeded their paternity had mated with a higher proportion of younger females. Young females may be more likely to lose the conceptus, or their offspring may suffer high postnatal mortality.     

The influence of artificial photoperiod on the growth,appetite and reproductive status of male red deer and sheep

Young male red deer and Suffolk X (Finn X Dorset) sheep were kept on an artificial photoperiod such that two cycles of daylength occurred during one calendar year. They were penned separately, fed to appetite, weighed weekly and measured tri-weekly.Both species showed two cycles of intake, growth and gonadal activity in response to the daylength when only one would have been shown on natural photoperiod, although in the sheep these cycles were of lower amplitude than in the deer. The deer grew two sets of antlers during the study. A lag of some 3–4 months occurred between an event such as peak food intake and the time it would have been expected to occur relative to the daylength cycle. It is considered that although daylength controls these cycles, there is an endogenous rhythm which photoperiod cannot completely suppress.     

Interaction effects between weather and space use on harvesting effort and patterns in red deer

Most cervid populations in Europe and North America are managed through selective harvesting, often with age‐ and sex‐specific quotas, with a large influence on the population growth rate. Less well understood is how prevailing weather affects harvesting selectivity and off‐take indirectly through changes in individual animal and hunter behavior. The behavior and movement patterns of hunters and their prey are expected to be influenced by weather conditions. Furthermore, habitat characteristics like habitat openness are also known to affect movement patterns and harvesting vulnerability, but how much such processes affect harvest composition has not been quantified. We use harvest data from red deer (Cervus elaphus) to investigate how weather and habitat characteristics affect behavioral decisions of red deer and their hunters throughout the hunting season. More specifically, we look at how sex and age class, temperature, precipitation, moon phase, and day of week affect the probability of being harvested on farmland (open habitat), hunter effort, and the overall harvest numbers. Moon phase and day of week were the strongest predictors of hunter effort and harvest numbers, with higher effort during full moon and weekends, and higher numbers during full moon. In general, the effect of fall weather conditions and habitat characteristics on harvest effort and numbers varied through the season. Yearlings showed the highest variation in the probability of being harvested on farmland through the season, but there was no effect of sex. Our study is among the first to highlight that weather may affect harvesting patterns and off‐take indirectly through animal and hunter behavior, but the interaction effects of weather and space use on hunter behavior are complicated, and seem less important than hunter preference and quotas in determining hunter selection and harvest off‐take. The consideration of hunter behavior is therefore key when forming management rules for sustainable harvesting.     

Parasite-induced risk of mortality elevates reproductive effort in male Drosophila.

A trade-off between sex and somatic maintenance is fundamental to life-history theory. Tests of this trade-off usually emphasize deleterious consequences of increased reproduction on life span. Here we show the reverse effect, that reductions in the expected life span elevate sexual activity. Experimentally parasitized male Drosophila nigrospiracula lived shorter lives, but before dying, they courted females significantly more than unparasitized controls. This greater courtship resulted in increased mating speed, and potentially greater reproductive success than parasitized males would have achieved otherwise. The results show that an environmental reduction in life span increases reproductive effort, and support the hypothesis of a trade-off between these key life-history traits.     

Testosterone and cortisol concentrations vary with reproductive status in wild female red deer

Although hormones are key regulators of many fitness and life history traits, the causes of individual level variation in hormones, particularly in wild systems, remain understudied. Whilst we know that androgen and glucocorticoid levels vary within and among individuals in mammalian populations, how this relates to key reproductive processes such as gestation and lactation, and their effects on a female''s measurable hormone levels are poorly understood in wild systems. Using fecal samples collected from females in a wild red deer population between 2001 and 2013, we explore how fecal androgen (FAM) and cortisol (FCM) metabolite concentrations change with age and season, and how individual differences relate to variation in reproductive state. Both FAM and FCM levels increase toward parturition, although this only affects FCM levels in older females. FCM levels are also higher when females suckle a male rather than a female calf, possibly due to the higher energetic costs of raising a son. This illustrates the importance of accounting for a female''s life history and current reproductive status, as well as temporal variation, when examining individual differences in hormone levels. We discuss these findings in relation to other studies of mammalian systems and in particular to the relatively scarce information on variation in natural levels of hormones in wild populations.     

The relationship between habitat choice and lifetime reproductive success in female red deer

In non-territorial species, individuals can move freely and should be distributed in an ideal free manner between habitats and areas with respect to resources that influence lifetime reproductive success (LRS). Consequently, no relationship between diet quality and LRS should be expected. However, there have been no attempts to test this prediction. The present paper investigates the relationship between forage habitat use and LRS in red deer (Cervus elaphus) hinds within three neighbouring areas on the Isle of Rum which differed in their amounts of high-quality-forage habitat. Within areas, hinds move widely and have access to the same resources. We found no correlation between LRS of individual hinds and their use of high-quality-forage habitat (i.e. short Agrostis/Festuca grassland). Our analysis suggests that high hind densities on short Agrostis/Festuca grassland offset any advantages of increased access to preferred forage. These results support the hypothesis that red deer hinds are distributed in an ideal free manner with respect to the use of high-quality-forage habitat. However, hinds rarely leave areas where they are born, and the analysis suggests that constraints in changing areas hindered an ideal free distribution on a larger spatial scale. Consequently, mean LRS was not the same within the three investigated areas: one area, with a low amount of short Agrostis/Festuca grassland and a low hind density, contributed more male offspring (and more total offspring) per hind to the population than the other two areas. Received: 11 September 1998 / Accepted: 15 March 1999     

Inbreeding alters context‐dependent reproductive effort and immunity in male crickets

Infection can cause hosts to drastically alter their investment in key life‐history traits of reproduction and defence. Infected individuals are expected to increase investment in defence (e.g., by increasing immune function) and, due to trade‐offs, investment in other traits (e.g., current reproduction) should decrease. However, the terminal investment hypothesis postulates that decreased lifespan due to infection and the associated reduction in the expectation for future offspring will favour increased investment towards current reproduction. Variation in intrinsic condition will likely influence shifts in reproductive investment post‐infection, but this is often not considered in such assessments. For example, the extent of inbreeding can significantly impact an individual's lifetime fitness and may influence its reproductive behaviour following a threat of infection. Here, we investigated the effects of inbreeding status on an individual's reproductive investment upon infection, including the propensity to terminally invest. Male crickets (Gryllodes sigillatus) from four genetically distinct inbred lines and one outbred line were subjected to a treatment from an increasing spectrum of simulated infection cue intensities, using heat‐killed bacteria. We then measured reproductive effort (calling effort), survival and immune function (antibacterial activity, circulating haemocytes and haemocyte microaggregations). Inbred and outbred males diverged in how they responded to a low‐dose infection cue: relative to unmanipulated males, outbred males decreased calling effort, whereas inbred males increased calling effort. Moreover, we found that inbred males exhibited higher antibacterial activity and numbers of circulating haemocytes compared with outbred males. These results suggest that an individual's inbreeding status may have consequences for context‐dependent shifts in reproductive strategies, such as those triggered by infection.     

Reduced reproductive effort in male field crickets infested with parasitoid fly larvae

Some populations of the field cricket Teleogryllus oceanicusare parasitized by the phonotactic fly Ormia ochracea. Flieslocate crickets by their song and deposit larvae onto them.The larvae develop inside the cricket for 1 week before killingthe host upon emergence. The reproductive compensation hypothesispredicts that parasitized crickets should increase their reproductiveeffort during the initial stages of infestation to offset theloss of fitness resulting from their shortened life span. An alternative hypothesis predicts that parasitized crickets willdecrease reproduction, either because they are unable to reproduceor because selection acting on the parasitoid favors decreasedhost reproduction. In laboratory experiments, parasitized malecrickets had reduced reproductive effort (spermatophore production,calling, mating activity, and mass allocated to reproductivetissue) compared to unparasitized males. Parasitized males fedad libitum showed no evidence of allocating a greater proportionof their resources to reproduction. Parasitized and healthymales did not differ significantly in resting or maximal metabolicrates, although this may have been due to the substantial contributionof larval respiration to the metabolic rate of the host—parasitoidcomplex. These results are consistent with previous studiesand suggest that T. oceanicus males parasitized by O. ochraceado not increase their reproductive effort. We discuss potentialreasons that crickets do not increase reproductive effort inresponse to fly larvae and address difficulties in demonstratingaltered life-history patterns in response to parasitism.