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1. The time at which animals enter puberty and become sexually mature is a significant life-history trait, influencing lifetime reproductive success. Great variation exists both between and within species.
2. The proximate mechanisms regulating the time at which a male enters puberty are not well-understood. Environmental cues are predicted to provide the relevant information on resource availability and opportunities for reproduction. When these are good the onset of puberty begins whereas at other times investment in survival becomes more important.
3. Male African striped mice (Rhabdomys pumilio) demonstrate large variation in the age at which they enter puberty, with grassland populations starting at 4 weeks old and semi-desert populations at over 10 weeks old.
4. We predicted that differences in the availability of food, social organization and population density could explain these differences.
5. Using data on 170 individual males from 4 years of field studies in a semi-desert population, we found that males became scrotal at a younger age when no breeding male was present in their group and when food was abundant, while population density had no effect.
6. In laboratory experiments we demonstrated that males fed with poor protein food, that regularly encounter larger unfamiliar males (mimicking high population density), and that live in family groups with their father present, become scrotal at a significantly later age, independent of their growth rate.
7. Males housed in family groups have lower testosterone but higher corticosterone levels than singly housed males, indicating they are sexually suppressed. When they become scrotal in their family group, their testes are only half as large as those of their singly housed brothers, and they contained significantly less sperm.
8. We conclude that male striped mice have a flexible response to the onset of puberty, and that the onset of sexual maturity is dependent on several environmental cues. Our results indicate that there is no threshold body mass, which, when reached, would automatically trigger puberty in male striped mice.
9. Male helpers in some species are reproductively suppressed, but ours is the first study that demonstrated the importance of different ecological factors in the timing of puberty in male helpers in a facultative cooperatively breeding species.
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The age at which animals reach sexual maturity is critical in determining an individual's lifetime reproductive success (Oli & Dobson 2003). If sexual maturity is reached too soon, resources that are more critical for survival might be wasted because reproduction at the animal's current state is unlikely or too costly (Berner & Blanckenhorn 2007). In contrast, if sexual maturity is reached too late, important opportunities to reproduce might be missed (Berner & Blanckenhorn 2007). The optimal time to reach sexual maturity can differ between species, as demonstrated by the slow–fast continuum differentiating species that mature, reproduce and die fast and species that take longer (Kraus et al. 2005; Read & Harvey 1989). Variation also exists within species (Waterman 2002; Yamamoto 1993) including humans (Belsky et al. 1991; Ellis & Garber 2000; Gluckman & Hanson 2006). Environmental and social stimuli might be important in determining the age at sexual maturity. However, the proximate mechanisms underlying the trade-off between the age at which to start puberty (also called maturation or adolescence) and the investment of resources into survival are poorly understood (Berner & Blanckenhorn 2007).
One species that shows large variation in the age at which males reach puberty and become sexually mature is the African striped mouse (Rhabdomys pumilio; Fig. 1). This species inhabits a variety of habitats from moist grasslands to semi-deserts. In grasslands, males can become scrotal (testes descended within the scrotal sac), indicating that they are sexually mature (Brooks 1982), at an age of only 4–6 weeks and a body mass between 20 and 30 g (Schradin & Pillay 2005b), whereas in the Succulent Karoo semi-desert scrotal males typically weigh more than 40 g and are more than 10 weeks old (Schradin & Pillay 2004, 2005b). Scrotality is necessary for the correct temperature for normal spermatogenesis (Hughes & Acerini 2008) and scrotal males are generally regarded as being in breeding condition and having viable sperm (for muroid rodents see Scheibler et al. 2006; Saltzman et al. 2006; for the striped mouse see Brooks 1982; Jackson & Bernard 1999; Jackson & Bernhard 2005; Perrin 1980a; Willan & Meester 1989). The age at which striped mouse males become scrotal for the first time is regarded as their age of onset of sexual maturity (Perrin 1980a; Brooks 1982; Willan & Meester 1989), but sexually mature adult striped mouse males are non-scrotal during the non-breeding season, when spermatogenesis is not necessary (Perrin 1980a; Willan & Meester 1989; Jackson & Bernard 1999; Jackson & Bernhard 2005; Schradin & Pillay 2005a). Population differences in the age of becoming scrotal are thought to be due to ecological and social differences between the populations (Schradin 2005). In grasslands, striped mice are solitary, population density is low and the breeding season is 6 months long (Perrin 1980a; Willan & Meester 1989). Thus, males born during one season can leave their natal group at 4–6 weeks of age and are able to start independent breeding (Schradin 2005). In contrast, in the Succulent Karoo, population density is high and the breeding season is only 3 months long. Here, striped mice typically form extended family groups with one breeding male, up to four breeding females, and adult philopatric males and females that do not breed in the group (Schradin & Pillay 2004). Groups can contain up to 30 adult individuals of both sexes (Schradin & Pillay 2004). Therefore males might not have the space to disperse in the same breeding season in which they were born due to the high population density. Moreover, in the Succulent Karoo the breeding season is typically only three months long (Schradin & Pillay 2005a), which does not allow much time for independent breeding in the breeding season a male is born. Additionally, young males might be suppressed by the dominant breeding male of the group, which can weigh more than 80 g (Schradin & Pillay 2004, 2005a), as well as by aggressive encounters with neighbouring territorial males and females (Schradin 2004; Schradin & Pillay 2004). Reproductive activity in striped mice is not influenced by the photoperiod (Jackson & Bernard 1999) but rather by food availability. In the Succulent Karoo, mice breed in spring when the photoperiod is relatively short, while grassland mice breed in summer, when the photoperiod is long (Schradin 2005). Thus, the variation in the timing when sexual maturity is reached might be caused by a combination of several factors which we tested using long-term field data and by conducting experiments in captivity. In particular, we tested the influence of the following three factors:
Figure 1. The striped mouse (Rhabdomys pumilio) occurs in many habitats in southern Africa. In the present study it was studied in the Succulent Karoo semi-desert, where it shows high social flexibility. The mice in the photograph are individually marked with hair dye, permanently marked with ear tags, and carry radio-transmitters.
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The influence of protein, which is known to affect growth and sexual maturity in many species (White 1993
). Reproduction in female striped mice is restricted to the period of availability of protein-rich food, such as insects in grasslands (Perrin 1980b
) and young plant growth in the Succulent Karoo (Schradin & Pillay 2006
). The protein content of food might also be an important cue for males regarding whether or not the breeding season continues, because females breed only during periods when protein rich food is abundant (Schradin & Pillay 2006
). Thus, we predicted that males with a protein poor diet would become scrotal at a later age than males with a protein rich diet.
The influence of social stress induced by high population density (Christian 1971
; Rödel et al. 2004
). When population density is high, small non-scrotal males are more likely to encounter larger aggressive territorial males. This could lead to increased levels of stress hormones which can suppress reproduction (Christian 1971
; Wingfield & Sapolsky 2003
). Thus, we predicted that males which are stressed by repeated encounters with larger, aggressive males would become scrotal at a later age than unstressed control males.
The potential of reproductive suppression within social groups. Philopatric males are known to have much higher corticosterone levels than breeding males (Schradin 2008b
; Schradin et al. 2009
), which could indicate that they are physiologically castrated (Reyer et al. 1986
; Creel 2001
; Wingfield & Sapolsky 2003
). Thus, we predicted that males housed in families would become scrotal at a later age than singly housed males.
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Using long-term data we have shown that free-living male striped mice in the Succulent Karoo semi-desert vary in the age when they reach puberty and become scrotal from 3 to 43 weeks, and a body mass from 13 to 65 g. Our study highlights the importance of long-term studies over a variety of ecological conditions, since in a previous one year study on the same population males were reported to become scrotal only when reaching a body mass of more than 40 g (more than 10 weeks old; Schradin & Pillay 2005b).
In most species, growth rate is one major factor determining the onset of puberty (Berner & Blanckenhorn 2007), and differences in growth rate could be the proximate mechanism leading to the observed differences in the age of puberty. However, in testing the influence of two factors we could demonstrate that males not only became scrotal at a later age, but also at a greater body mass. Males stressed by encounters with unrelated males, and males housed with their father in their family, did not reach a threshold body mass of entering puberty at a later age. Instead, they became scrotal at a higher body mass. In contrast to this pattern were males subjected to a poor protein diet; these males grew slower than control males and became scrotal at a later age, but even significantly lower body mass! Similarly, males housed in mother families became scrotal at a lower body mass (but not younger age), possibly due to competition for food within the family. In the field, body mass of males becoming scrotal was highly variable. These results indicate that there is no threshold body mass, which, when reached, automatically triggers puberty in male striped mice.
Typically, organisms must acquire a minimum amount of resources and body mass before they can start puberty (Berner & Blanckenhorn 2007). In our study, some male striped mice entered puberty at an extremely early age of 3 weeks. This indicates that male striped mice can enter puberty shortly after they are weaned (16 days; Brooks 1982). It appears that male striped mice do not have to acquire resources before entering puberty, but rely on environmental information indicating that sufficient resources will be available to go through puberty. Thus, the striped mouse shows extraordinary flexibility in its ontogenetic pathways, enabling it to follow a strategy of rapid maturation and reproduction or a strategy of slow maturation and reproduction.
As predicted, males fed a poor protein diet became scrotal at a later age. One co-factor was that males fed sunflowers had not only access to more protein, but also to more fat, as sunflowers have a much higher fat content than carrots and apples. Thus, it was high quality food that influenced the age when males became scrotal, and several previous studies indicate that it is protein which is important for striped mice. For example, the availability of protein rich food determines the breeding season in striped mice (Perrin 1980b; Schradin & Pillay 2006) and experimental provisioning of food during the non-breeding season (winter) increases testes mass and sperm storage (Jackson & Bernard 2005). In contrast to many other mammals, reproduction and the excretion of hormones related to reproduction are not influenced by photoperiod in striped mice (Jackson & Bernard 1999; Schradin 2008a). Instead, dietary protein might influence endocrine pathways and gonadal function (Schneider 2004; Schoech et al. 2004). This relationship has been demonstrated in Florida scrub-jays (Aphelocoma coerulescens), where artificial provisioning of high protein food leads to higher testosterone and lower corticosterone levels, and earlier onset of breeding (Schoech et al. 2004). Adult male striped mice become non-scrotal during the non-breeding season (Schradin & Pillay 2005a) when they decrease their testosterone levels and increase their corticosterone levels (Schradin 2008b). The same endocrine mechanisms are likely to act in young males.
Males became scrotal at a later age when they experienced social stress by meeting larger unknown males. Five encounters a week was probably much less than what young males would experience under conditions of high population density in the field, when there are more than 150 adult mice per ha (Schradin & Pillay 2005a) and aggressive territorial encounters are frequent (Schradin 2004; Schradin & Pillay 2004). These encounters might lead to increased secretion of glucocorticoids, which could suppress reproduction (Wingfield & Sapolsky 2003).
Family housed males became scrotal much later than singly housed males. In the field, males in groups without a breeding male became scrotal at a younger age than males living with a breeding male. In captivity, when the father was removed but the mother remained, males became scrotal as the same age as their singly housed brothers. In contrast, when the mother was removed but the father remained, males became scrotal later. Thus, results from the field and the laboratory studies indicate reproductive suppression by the father.
From field studies, we know that philopatric males have much higher corticosterone levels than breeding males (Schradin 2008b; Schradin et al. 2009), which could indicate that they are physiologically castrated (Reyer et al. 1986; Creel 2001; Wingfield & Sapolsky 2003). However, non-scrotal males did not have higher serum corticosterone levels than their brothers in the week their brothers became scrotal. Only a few weeks later, when the family housed males also became scrotal, family housed males had nearly twice as high corticosterone levels when compared to their brothers, which had decreased their corticosterone levels in the meantime. Corticosterone levels of family house males were somewhat lower (1200 ng/mL) than those of philopatric free living males (2000 ng/mL; Schradin 2008b), while levels of singly housed males were similar to those of free living roaming and breeding males (Schradin et al. 2009). This indicates that high corticosterone levels alone do not prevent males from becoming scrotal.
Family housed males had much lower serum testosterone levels than singly housed males. Even when they were scrotal, their testosterone levels did not increase, but were three times lower than those of their brothers. Furthermore, scrotal family housed males had much smaller testes than singly housed males, and 79% of scrotal family housed males had no sperm at all. This indicates that family housed males might have been sexually suppressed and physiologically castrated (Reyer et al. 1986; Creel 2001; Wingfield & Sapolsky 2003; Young et al. 2006).
In cooperative breeding societies, helpers often have lower androgen levels than breeders (Oliveira et al. 2003, 2008), though this not the case in all species. For example male helpers of red-cockaded woodpeckers have high testosterone levels and seem capable of breeding (Khan et al. 2001), as do helpers of azure-winged magpies (Cyanopica cyanus, Cruz et al. 2003). Similarly, in the cooperatively breeding cichlid Neolamprologus pulcher, a male helper's reproduction is not suppressed and their androgen levels are similar to those of breeders when kept in captivity (Oliveira et al. 2003). However, for the same species evidence exists from the field that helpers are sexually suppressed, as their testes were much smaller than those of breeders (Fitzpatrick et al. 2006). Male meerkat (Suricate suricatta) helpers have high testosterone levels and are capable of breeding, though they do so only with females from neighbouring groups (Young et al. 2005). In cooperatively breeding common marmosets (Callithrix jacchus), subordinate males do not suffer from suppression of testosterone secretion, even though dominant males typically have the highest testosterone levels (Abbott 1984). Regarding glucocorticoids, the pattern is similarly diverse: in some cooperatively breeding species breeders have high levels, indicating costs of dominance, while in other species helpers have high levels, indicating stress and reproductive suppression (Creel 2001). In sum, variation exists between different cooperatively breeding species in the amount to which male helpers are reproductively suppressed. However, very little is known about the time male helpers reach puberty in cooperative breeding societies, and future studies on other species would be important.
Here we were able to demonstrate different factors that delay the age of becoming scrotal in the striped mouse. However, each experiment taken individually cannot explain the pattern observed in nature, where some males of the Succulent Karoo only became scrotal when their body mass was greater than 40 g (Schradin & Pillay 2005b). The three factors might act together in the field, and males became scrotal at a later age when they lived in family groups with a dominant breeding male, when they experienced numerous aggressive encounters with neighbours, and when protein rich food vanished quickly during the short breeding season. However, when food was plentiful and no dominant breeding male was present, males became scrotal at a very young age. Thus, the combination of several factors under natural conditions can explain the variability observed in nature.
In conclusion, many factors determine when a male striped mouse becomes scrotal. Striped mice can follow either a mature, reproduce and die fast strategy or a mature, reproduce and die late strategy. It has been demonstrated that the striped mouse shows extraordinary flexibility in its social behaviour, ranging from solitary living to extended family groups with communal breeding and helpers at the nest (Schradin & Pillay 2004, 2005b), enabling it to adapt to different ecological conditions (Schradin 2005). Here we showed that this flexibility is also present in male reproductive maturation. Our study implies that male striped mice are able to use several environmental cues to reach sexual maturity at an optimal age.