Evolution of variation in male secondary sexual characteristics

Summary The male pied flycatcher Ficedula hypoleuca exhibits sexual dimorphism in its plumage colour, varying from a female-like brown to jet black. The evoltution of this variation in male plumage colour can be explained by at least eight hypotheses viz., (I) neutral mutation; (II) individual recognition; (III) three forms of inter-sexual selection; (IIIa) mate selection for phenotypes, (IIIb) Fisherian selection, (IIIc) handicap selection; (IV) intrasexual selection; (V) delayed maturation; and (VI) female mimicry. The assumptions and predictions derived from all these hypotheses were tested by analysing the observed variation in male plumage colour in relation to age, body size, physical condition, survival rate, aggressivity in territorial defence, territorial quality, female choice of mate, sex ratio, and reproductive success. We found that: males became blacker with age; black males were larger than browner ones; however, browner males survived better between breeding seasons than did blacker ones; black males were more aggressive against black than brown intruders; blacker males occupied better territories; blacker males were paired earlier than browner males; and finally blacker males produced heavier offspring than did brown males. A reasonable conclusion from the results of these analyses is that four of the hypotheses considered, viz. mate selection for phenotypes (IIIa), Fisherian selection (IIIb), handicap selection (IIIc), and intra-sexual selection (IV) could not be rejected. We therefore suggest that the evolution of the observed variation in the secondary sexual characteristics of the male pied flycatcher can be explained by a combination of these hypotheses.     

Progress in the ecology and conservation of giant pandas

Giant panda (Ailuropoda melanoleuca) conservation is a possible success story in the making. If extinction of this iconic endangered species can be avoided, the species will become a showcase program for the Chinese government and its collaborators. We reviewed the major advancements in ecological science for the giant panda, examining how these advancements have contributed to panda conservation. Pandas’ morphological and behavioral adaptations to a diet of bamboo, which bear strong influence on movement ecology, have been well studied, providing knowledge to guide management actions ranging from reserve design to climate change mitigation. Foraging ecology has also provided essential information used in the creation of landscape models of panda habitat. Because habitat loss and fragmentation are major drivers of the panda population decline, efforts have been made to help identify core habitat areas, establish where habitat corridors are needed, and prioritize areas for protection and restoration. Thus, habitat models have provided guidance for the Chinese governments’ creation of 67 protected areas. Behavioral research has revealed a complex and efficient communication system and documented the need for protection of habitat that serves as a communication platform for bringing the sexes together for mating. Further research shows that den sites in old‐growth forests may be a limiting resource, indicating potential value in providing alternative den sites for rearing offspring. Advancements in molecular ecology have been revolutionary and have been applied to population census, determining population structure and genetic diversity, evaluating connectivity following habitat fragmentation, and understanding dispersal patterns. These advancements form a foundation for increasing the application of adaptive management approaches to move panda conservation forward more rapidly. Although the Chinese government has made great progress in setting aside protected areas, future emphasis will be improved management of pandas and their habitat.     

Seasonal variation in ejaculate traits of male red-winged blackbirds (Agelaius phoeniceus)

Many reproductive traits, including ejaculate characteristics, usually show remarkable seasonal variation, but the potential for such dynamics in sperm morphology has been overlooked. Several studies have revealed high within-male repeatability in sperm morphology, but samples have typically been collected within a few hours or days, and the consistency of sperm morphology over longer periods remains unexplored. Here, we tested whether ejaculate traits, including sperm morphology, sperm number, and sperm velocity, exhibit seasonal phenotypic plasticity in a long-lived seasonal breeder, the red-winged blackbird (Agelaius phoeniceus). We found absolute and/or relative flagellum length and sperm velocity to increase across the season, whereas sperm numbers within ejaculates declined. Sperm morphological traits were further positively associated with harem size or the total number of offspring that fledged in each male’s territory, suggesting that sperm morphology is likely to be linked to male reproductive quality. The underlying mechanisms of these patterns of seasonal variation remain unresolved, but we discuss our results in the context of dynamics of reproductive hormones, testicular structures and function, and reproductive behavior.     

Limited geographic variation in the acoustic structure of and responses to adult male alarm barks of African green monkeys

The global diversity of human languages is a remarkable feature of our species, which requires a capacity for rapid vocal learning. Given that primate alarm calling systems have played an important role in the language origin debate, identifying geographic variation in primate alarm calls and understanding the underlying causal mechanisms are important steps to help uncover evolutionary precursors to language. This study investigates geographic variation in the alarm bark of the widely distributed African green monkey (Chlorocebus). To quantify geographic variation in spectral and temporal call structure, acoustic analysis was used to compare the adult male barks of green monkeys (Chlorocebus sabaeus) and two subspecies of vervet (Chlorocebus pygerythrus pygerythrus and Chlorocebus pygerythrus hilgerti). Playback experiments were also carried out to test whether adult male vervets would distinguish between the barks of own-group males, unknown conspecific males and green monkey males. Acoustic analysis showed that, whilst similar in overall structure, the barks of green monkeys could be distinguished from vervet barks with a high degree of accuracy; the barks of vervet subspecies could also be discriminated, although to a lesser degree. Males responded most strongly to unknown conspecific males’ barks, and exhibited responses typical of leopard-avoidance and territorial defence. Taken together, these findings indicate that variation in alarm calls can be best explained by phylogenetic distance, and that intra- and inter-species differences are relevant during social interactions. Moreover, barks may function as an alarm and display call, which could explain the observed sexual dimorphism in barks in this genus.     

Reproductive competition and fecal testosterone in wild male giant pandas (<Emphasis Type="Italic">Ailuropoda melanoleuca</Emphasis>)

The giant panda (Ailuropoda melanoleuca) is notoriously difficult to study in the wild, but its interesting reproductive ecology makes the effort worthwhile. Perhaps more than most species, the panda is energy-limited, which alters the cost/benefit analysis of its reproductive ecology. Using global positioning system/very high frequency radiocollars to locate mating aggregations, we used behavioral observations and fecal testosterone assays to gain insight into male panda reproductive effort and strategies, and test theories relating to reproductive competition. Male pandas initially competed fiercely for access to females that were about to be fertile, but once male competitive status was determined, aggression rates declined. Contact aggression was only observed during the first 2 days of mating aggregations; thereafter, it was replaced with noncontact aggression and avoidance. Agonistic interactions were highly asymmetrical, with contest losers (subordinates) showing less aggression and more avoidance than contest winners (dominants), both before and after contest outcome was established. The competitively superior male displayed mate-guarding tactics and secured all observed copulations. Contrary to theoretical predictions, testosterone levels did not predict aggression levels or contest winners and also were not affected by winning or losing a contest. Body size appeared to be the primary determinant of contest outcome. We discuss our findings in light of theoretical predictions, such as those arising from the “challenge hypothesis,” in the context of the giant panda’s foraging and nutritional ecology.     

Phenotypic differentiation in female preference related to geographic variation in male predation risk in the Trinidad guppy (Poecilia reticulata)

Summary Populations of the Trinidad guppy range from areas with high levels of predation by other species of fish to areas with little or no piscine predation. Previous studies have shown that variation among populations in male coloration can be explained by a balance between female preference for brighter males and natural selection against bright males. High levels of male courtship activity may also increase both predation risk and mating success. Therefore, in high-predation areas, females that mate with males that court frequently as well as those that choose bright males would presumably produce male offspring with low survivorship. Consistent with this variation in natural selection, we observed that females from high-predation populations were less likely to choose bright and frequently courting males than females from low-predation populations. This result supports the hypothesis that female preference is evolving as a character genetically correlated with the preferred male character, in which case higher levels of natural selection acting against the male character should be related to lower levels of female preference.     

Sexual selection and variation in reproductive strategy in male yellow warblers (Dendroica petechia)

Summary Male yellow warblers (Dendroica petechia) exhibit extensive variation in the amount and conspicuousness of the sexually distinctive brown streaking on the breast. We investigated this intraspecific variation in degree of sexual dichromatism to see if male plumage rank (essentially the amount of brown streaking) is correlated with the amount of reproductive effort allocated to parental investment, as sexual selection theory would predict. As predicted, the average rate of feeding visits to the nest by males was negatively correlated with the plumage rank of the male in 1982 (Fig. 1) and 1983 (Fig. 2), and varied little between years or among study areas. Within one study area, the higher nest visit rate of dull (low plumage rank) males was correlated with higher nestling growth rates. But in the other two study areas, where bright (high plumage rank) males predominated, nestlings of bright males tended to have the highest growth rates despite minimal nest visit rates. Thus, overall there was no correlation between male plumage rank and nestling growth rate, a potential index of relative reproductive success, in either year (Figs. 3 and 4). This overall equal nest success likely helps to maintain the behavioral and plumage polymorphism. Since we could find no evidence that the high nestling growth rates of bright males were due to an adjustment of female parental effort to compensate for low male parental effort, there must be some other benefit of being bright which contributes to nest success. To address this, we used the relationship between parental feeding rates and nestling growth rates for each nest as an index of relative territory quality. This analysis suggests that bright males generally occupy the best territories available, possibly because they are more aggressive in obtaining and defending them than dull males. Dull males appear to be relegated to poorer territories, where an increase in male parental contribution would be necessary to achieve high nestling growth rates. We propose that different males are using alternative but evolutionarily stable reproductive strategies, in a way that is consistent with the predictions of sexual selection theory. Allocation of limited reproductive effort to parental investment decreases as sexual dichromatism increases, which probably reflects an increased investment in intermale competition for the best territories.     

Sources of variation in male mating success and female oviposition rate in a nonterritorial dragonfly

Summary Variance in male mating success and female oviposition rate was studied on a lifetime and daily scale in a nonterritorial libellulid dragonfly. While controlling for weather, population density, and sex ratio, we investigated whether phenotypic variation could explain a significant amount of the observed variation. By collecting most of the data in a large outdoor field enclosure, we had access to (1) real lifetime data as emigration was prevented, (2) exact values of density and sex ratio, and (3) phenotypic data that are virtually unavailable under natural conditions. Variance in LMS was higher in males than variance in lifetime number of ovipositions in females. Lifespan was of major importance in explaining the variation. Males readily remated on the same day whenever possible (maximum 6 times), whereas in females each oviposition bout usually was followed by a nonreproductive period of approximately 4 days. An analysis of the sources of variance in daily reproduction rate showed that, besides the expected effects of weather, an excess of one sex resulted in a negative effect on the individual mating probability of members of that sex. Even after correction for weather and population parameters, phenotypic traits explained a significant amount of the remaining variation: males with a high mating rate were large, agonistic, active mate searching, and long-living individuals. Females were more likely to oviposit when they showed higher flight activity and when more days had elapsed since the previous oviposition. The presence of a strong size effect on male mating probability, and its absence in females, was confirmed at a pond (native habitat). We propose a model on the causal relationships between the relevant parameters and the variation in reproductive success. Finally, we briefly discuss why variance in reproductive success is not a very good measure of the opportunity for sexual selection in this species. Offprint requests to: N.K. Michiels at the present address     

Potential solar radiation pattern in relation to the monthly distribution of giant pandas in Foping Nature Reserve, China

Solar radiation is an important parameter in ecological process modeling, hydrological modeling and bio-physical modeling. However, models focusing on solar radiation in relation to giant panda habitat and seasonal distribution are limited. The research aims to form spatial models of 12 month solar radiation patterns and to investigate the relation between the solar radiation patterns and the monthly distribution patterns of giant pandas. The solar radiation model of Kumar et al. was adopted for this study in Foping Nature Reserve (NR), China. By comparing twelve monthly solar radiation patterns and calculating statistics such as maximum, minimum, mean and standard deviation of the solar radiation, diversified solar radiation patterns over different months were obtained. Maximum solar radiation occurred in June and July, while minimum solar radiation occurred in December and January. The annual sum of solar radiation was 6954 MJ/m² in Foping NR. The range in solar radiation was smaller in hot months and larger in cold months. Radio tracking data of giant pandas were collected for twelve months and the ensuing maps were overlaid with the twelve-month solar radiation map to analyze the relation between the giant panda's monthly distribution and solar radiation. Our results showed that giant pandas prefer areas with lower solar radiation in warm months and select areas with higher solar radiation in cold months, which illustrates that the distribution of giant pandas is indeed affected by solar radiation. To a certain degree, it also explains the behavior of seasonal movement by giant pandas in Foping NR.     

Effects of extreme variation in female morph frequencies on the mating behaviour of male damselflies

Female-limited polymorphism is often attributed to selection to avoid excessive male mating attempts. It is encountered in various taxonomic groups, but is particularly common in damselflies, where one female morph (andromorph) typically resembles the conspecific male in colour pattern, while the other(s) (gynomorph(s)) do not. Two sets of theories have been proposed to explain the phenomenon in damselflies, which can be classified as the learned mate recognition (LMR) and male mimicry (MM) hypotheses. To test predictions of these hypotheses, we evaluated the rate of male sexual response towards female morphs and conspecific males in the damselfly Nehalennia irene. The LMR hypothesis predicts that males should respond sexually to andromorphs at greater rates in populations containing a higher relative frequency of andromorphs. The MM hypothesis predicts that males respond more often sexually to both andromorphs and males as the ratio of andromorphs to males increases. While LMR predicts that the rate of mating attempts towards gynomorphs should vary, the MM predicts that it should be relatively fixed. On experimentally presenting live specimens to focal males in five different populations with extreme variation in female morph frequencies, we observed that as the andromorph frequency and ratio of andromorphs to males increased, the proportion of male mating attempts increased on both andromorphs and males, whereas it decreased on gynomorphs. While the simplest form of the MM hypothesis is rejected, the results support specific predictions of both hypotheses and suggest that future studies should not treat these hypotheses as mutually exclusive.     

Population frequencies of alternative male phenotypes in tree lizards: geographic variation and common-garden rearing studies

Tree lizards (Urosaurus ornatus) vary in throat fan (dewlap) color. Earlier, we described five dewlap types (Orange, Orange-Blue, Yellow, Yellow-Blue, and Blue), and reported that only males had blue in the dewlap and that presence or absence of a discrete blue patch was correlated with male alternative reproductive phenotypes in a central Arizona population. Here, with a modified scheme characterizing two dewlap elements, background color (orange, yellow, blue) and blue patch occurrence, we assessed: (1) sexual, annual, and geographic variation in the frequencies of dewlap elements; (2) simple habitat correlates; and (3) the effects of laboratory rearing regime on dewlap type. Within a population, frequencies of males and females expressing orange or yellow backgrounds did not differ, suggesting that control of background is similar in the sexes. Within several populations, frequencies of the dewlap elements did not differ across years (and probably generations), indicating that phenotype frequencies are relatively stable. Among five populations frequencies of background colors varied, as did frequencies of male types (blue patch present or absent). Dewlap frequencies did not correlate with habitat (boulders or mesquite trees), although few populations were sampled. In male and female offspring reared from eggs to sexual maturity in a common-garden laboratory study, background color frequencies in both sexes and blue patch frequencies in males differed among offspring from different populations. Offspring frequencies matched respective parental population frequencies. Results suggest that among-population variation in frequencies of the two dewlap elements are mediated by differences in genetics, in maternal effects, or both. Thus, differences in male behavior functionally linked to the blue patch also may be controlled by genetic or maternal effects. Received: 17 January 1997 / Accepted after revision: 30 August 1997     

Interpopulational variation in chemosensory responses to selected steroids from femoral secretions of male lizards, Podarcis hispanica, mirrors population differences in chemical signals

Chemical signals are important for mate and species recognition. If variation in chemical signals occurs between populations of the same species, these differences could later preclude mating between populations and lead to speciation. In the Iberian wall lizard, Podarcis hispanica, the lipophilic fraction of femoral secretions of males is mainly a mix of steroids and fatty acids. Among steroids, the most abundant compounds are cholesterol and cholesta-5,7-dien-3-ol, which are implicated in intraspecific communication and sexual selection. Interpopulational differences in chemical signals of males, and in response to these chemicals, could contribute to reproductive isolation between populations, which would explain the known genetic differences between these populations. Chemical analyses indicated that five distinct populations of this lizard from Madrid (Central Spain) differed in the proportions of two steroids (cholesterol and cholesta-5,7-dien-3-ol) in femoral secretions. Moreover, lizards discriminated and had high chemosensory responses (i.e., high tongue-flick rates) to these steroids, but showed interpopulational differences. Lizards from populations with cold temperatures and high relative humidity (i.e., northern Madrid) elicited higher responses to these steroids, whereas the converse occurred for lizards from populations occupying dry and hot habitats (i.e., southern Madrid). Interestingly, the magnitude of the chemosensory responses to cholesta-5,7-dien-3-ol in each population mirrored the abundance of this compound in secretions of males of that population. These results suggest that the importance of cholesta-5,7-dien-3-ol in males’ secretions might be lower for lizards from the southern populations. These differences in the relative importance of chemical signals could explain reproductive isolation and cryptic speciation between populations of this lizard.     

Frequency-dependent male mate harassment and intra-specific variation in its avoidance by females of the damselfly Ischnura elegans

We focused on male harassment on different female color morphs of the damselfly Ischnura elegans and on variation in morph-specific mating avoidance tactics by females. In I. elegans, one of the female morphs is colored like the conspecific male (andromorphs) while the other morphs are not (gynomorphs). Our first goal was to quantify morph-specific male mating attempts, hence male harassment, in populations with manipulated population parameters (densities, sex ratios, and proportion of andromorphs). Second, we examined the female's perspective by looking for potential differences in morph-specific mating avoidance tactics and success of those tactics in a natural population. Differences in population conditions did influence the number of male mating attempts per morph. The less frequent female morph was always subject to fewer mating attempts, which contradicts earlier hypotheses on mimicry, but supports those that assume that males learn to recognize female morphs. Gynomorphs occupy less open habitat and often fly away when a male approaches, while andromorphs use more open habitat, do not fly large distances and directly face approaching males. Female morphs did not differ in the proportion of successful mating-avoidance attempts. Our results suggest that the maintenance of the color polymorphism is most probably the result of interactive selective forces depending on variation in all population conditions, instead of solely density- or frequency-dependent selection within populations.     

Seasonal variation and social correlates of androgen excretion in male redfronted lemurs (Eulemur fulvus rufus)

The aim of this study was to examine effects of seasonal and social factors on male androgen excretion in a seasonally breeding primate living in multimale-multifemale groups. By combining detailed behavioural observations (>2,500 h) on 3 groups of redfronted lemurs living in Kirindy Forest/Madagascar with non-invasive hormone analysis of >800 faecal samples collected concomitantly from the same animals, we tested predictions on: (1) the effect of social status on immunoreactive testosterone (iT) excretion; (2) seasonal variation of iT across reproductive periods; and (3) the relationship between aggression and iT excretion. The study lasted 14 months, covering two mating and one birth season. The results revealed that males fall into two distinct social classes, with one dominant male and several subordinate males in each group. In contrast to our prediction, the behavioural differences between these two classes were not reflected by differences in androgen levels, making physiological suppression of testicular function an unlikely mechanism of male reproductive competition. As expected for a seasonally breeding animal, iT values were elevated during the mating season. Androgen levels tracked the increase in the rate of reproductive aggression during the mating season as predicted by the challenge hypothesis. An increase in aggression due to spontaneous social instability outside the mating season, however, was not linked to a parallel rise of iT. Furthermore, the highest iT levels were obtained during the birth season, which may be part of a male strategy to remain aggressive during this period of high infanticide risk. These findings suggest that redfronted lemurs do not respond with increases in androgens to short-term challenges and that high androgen levels instead correlate with longer-lasting and predictable situations, such as the mating and birth seasons.     

Ecological responses to variation in seasonal snow cover

Seasonal snow is among the most important factors governing the ecology of many terrestrial ecosystems, but rising global temperatures are changing snow regimes and driving widespread declines in the depth and duration of snow cover. Loss of the insulating snow layer will fundamentally change the environment. Understanding how individuals, populations, and communities respond to different snow conditions is thus essential for predicting and managing future ecosystem change. We synthesized 365 studies that examined ecological responses to variation in winter snow conditions. This research encompasses a broad range of methods (experimental manipulations, measurement of natural snow gradients, and long-term monitoring), locations (35 countries), study organisms (plants, mammals, arthropods, birds, fish, lichen, and fungi), and response measures. Earlier snowmelt was consistently associated with advanced spring phenology in plants, mammals, and arthropods. Reduced snow depth often increased mortality or physical injury in plants, although there were few clear effects on animals. Neither snow depth nor snowmelt timing had clear or consistent directional effects on body size of animals or biomass of plants. However, because 96% of studies were from the northern hemisphere, the generality of these trends across ecosystems and localities is also unclear. We identified substantial research gaps for several taxonomic groups and response types; research on wintertime responses was notably scarce. Future research should prioritize examination of the mechanisms underlying responses to changing snow conditions and the consequences of those responses for seasonally snow-covered ecosystems.     

Seasonal variation in the relationship between cellular immune response and badge size in male house sparrows (Passer domesticus)

The immunocompetence handicap hypothesis postulates that secondary sexual traits are honest signals of male quality because steroid hormones (such as corticosteroids and sex steroids), which are supposed to favor the development of secondary sexual traits, may also have immunosuppressive effects. Certain secondary sexual traits are not only used as mate choice signals but also play a role as badges of status. In the house sparrow (Passer domesticus), males have a bib of black feathers which is used both as a signal of social status in male-male interactions and by females when choosing a mate. We investigated the relationships between bib size and cellular immune response in male house sparrows during and outside the reproductive season. Males with large badges were found to have lower levels of immunocompetence, as assessed using a T-cell-mediated immunity assay, during the reproductive season, as predicted by the immunocompetence handicap hypothesis. Conversely, in November, the correlation between badge size and cellular immune response was positive, possibly reflecting the better access to trophic resources of large-badged dominant males in winter flocks. Received: 24 September 1998 / Received in revised form: 2 February 1999 / Accepted: 14 February 1999     

Innate responses to male sexual harassment in female mosquitofish

Male mosquitofish are very persistent in their sexual activity and harass any female they encounter. Gravid females pay a large tribute to this intense male sexual activity in terms of reduced foraging efficiency. Previous observations have demonstrated that gravid females, when chased by a male, dilute male harassment by moving closer to other females to form shoals. They also approach other males to promote male competition, and when males differ in size, they preferentially target large males, whose harassment is less intense. In this study, we tested whether the modulation of females’ social preferences in response to male harassment is innate or learned. We tested social preference in three groups of females that differed in experience of sexual harassment and in the factors affecting it. Females of the first group were reared without any sexual experience, and pregnancy was induced through artificial insemination. The second group was composed of naive females kept singly with a male; these females experienced sexual harassment but were prevented from experiencing the effects of male–male competition and shoaling on the amount of male sexual harassment. In the third group (controls), females were reared in multi-male, multi-female groups and could experience the modulating effects of social interactions on sexual harassment. When exposed to a harassing male, females of the three groups immediately reduced their distance from another female, approached a group of males or moved toward the larger of two available males. Moreover, the results for these three groups of females were similar to those obtained in wild-caught females that were tested in the same three tests in a previous study (Dadda et al. An. Behav., 70:463–471, 2005). This suggests that the strategies adopted by females in response to male sexual harassment do not need to be learned through specific experience of the social contexts.