Examining the social landscapes of alternative reproductive strategies

Social environments are inherently dynamic, often changing depending on the frequency and outcomes of conspecific interactions – they can be simultaneously the targets and agents of selection. Understanding how organisms settle in heterogeneous social environments and the effects this has on reproductive success is vital to our understanding of the selective forces at work in wild populations. From an intensive behavioural and ecological study of territoriality in the polymorphic white‐throated sparrow (Zonotrichia albicollis), we demonstrate that males of the two morphs inhabit social niches that correspond to their respective alternative reproductive strategies. By integrating molecular ecology and Geographic Information Systems, we generated continuous, socio‐spatial models of local conspecific density and cuckoldry risk. Our results suggest that the morphs segregate their territories based on socio‐spatial variables, creating a heterogeneous social landscape that matches each behavioural phenotype with a favourable social environment. Specifically, the monogamous tan males tended to settle in low‐density areas that were also low for cuckoldry risk, while the opposite was true for the promiscuous white males. This pattern of socio‐spatial heterogeneity, combined with the social niche partitioning we observed, might act as a social niche polymorphism, and play an important role in maintenance of the alternative reproductive strategies of the white‐throated sparrow. Socio‐spatial factors, similar to those observed in the white‐throated sparrow, may play important roles in the evolution of mating systems in other species, even those with more continuous or cryptic variation.     

An experimental test for alternative reproductive strategies underlying a female-limited polymorphism

Polymorphism often corresponds to alternative mating tactics in males, but much less is known about this relationship in females. However, recent work suggests that selection for alternative reproductive strategies in females can maintain genetic variation in important life-history traits. Brown anole lizards (Anolis sagrei) exhibit a genetically based polymorphism in dorsal pattern that is expressed only by females, which occur in bar (B), diamond (D) and intermediate diamond-bar (DB) morphs. Here, we use a combination of natural history data, captive breeding studies and phenotypic manipulations of reproductive investment to test the hypothesis that this polymorphism corresponds to morph-specific patterns of reproductive investment. Three years of data from wild females and two generations of captive breeding revealed no differences among morphs in the frequency of egg production or in the number, frequency, size or sex ratio of offspring. Manipulations of reproductive investment via surgical ovariectomy revealed significant costs of reproduction with respect to survival, growth, immune function and haematocrit, but the magnitudes of these costs did not differ among morphs. Collectively, our results refute the hypothesis that this sex-limited polymorphism is maintained by selection for alternative reproductive strategies. We compare this finding to other systems in which polymorphic females exhibit alternative reproductive tactics and discuss other selective factors that could maintain polymorphism in anoles.     

Alternative male reproductive strategies in the peacock blenny

A 4-year study (1989–1992) of a population of Lipophrys pavo living in a brackish lagoon (Maugio, France) revealed three types of male during the spawning season (April to September): (i) nest-breeder males which are territorial, and have well-developed secondary sexual characteristics; (ii) non-functional males which were abundant only in 1991 when population density was very high and (iii) 1-year-old kleptogamic males with small body size which possess neither secondary sexual organs nor a testicular gland, although their testes are functional and hyperdeveloped (up to 10.5% of carcass weight). The percentage of kleptogamic males was fairly stable in the population (from 7.9 to 10.0%) and highly variable in their age class (from 8.5 to 51.3%). It is suggested that kleptogamy is a conditional strategy adopted by smaller males.     

Subordinate male meerkats prospect for extra-group paternity: alternative reproductive tactics in a cooperative mammal

In cooperatively breeding species, subordinates typically suffer strong constraints on within-group reproduction. While numerous studies have highlighted the additional fitness benefits that subordinates might accrue through helping, few have considered the possibility that subordinates may also seek extra-group matings to improve their chances of actually breeding. Here, we show that subordinate males in cooperative meerkat, Suricata suricatta, societies conduct frequent extraterritorial forays, during periods of peak female fertility, which give rise to matings with females in other groups. Genetic analyses reveal that extra-group paternity (EGP) accrued while prospecting contributes substantially to the reproductive success of subordinates: yielding the majority of their offspring (approx. 70%); significantly reducing their age at first reproduction and allowing them to breed without dispersing. We estimate that prospecting subordinates sire 20-25% of all young in the population. While recent studies on cooperative birds indicate that dominant males accrue the majority of EGP, our findings reveal that EGP can also arise from alternative reproductive tactics employed exclusively by subordinates. It is important, therefore, that future attempts to estimate the fitness of subordinate males in animal societies quantify the distribution of extra-group as well as within-group paternity, because a substantial proportion of the reproductive success of subordinates may otherwise go undetected.     

Relative fitness of alternative male reproductive tactics in a mammal varies between years

1. In many species, males can use different behavioural tactics to achieve fertilization, so-called alternative reproductive tactics (ARTs). Few field studies have measured fitness consequences of ARTs under varying environmental conditions. 2. Here, we describe fitness consequences of three phenotypically plastic ARTs in the African striped mouse (Rhabdomys pumilio) and show that relative fitness of ARTs differs between years. Each year represents a different generation. 3. For the generation living under high population density, tactics differed in relative fitness in accordance with the theory of conditional strategies, with highly successful territorial breeding males having 10 times higher success than solitary roaming males and 102 times higher success than adult natally philopatric males. 4. For the generation living under intermediate population density, the territorial breeding and roaming tactics yielded similar fitness, which would be in agreement with the theory of mixed strategies. No philopatric males occurred. 5. For the generation living under low population density, roaming was the only tactic used and some roamers had very high fitness. 6. The main prediction of status-dependent selection for conditional strategies is a correlation between fitness and status, often measured as body mass, but we did not find this correlation within tactics when more than one tactic was expressed in the population. 7. Female distribution seems to have an effect on which reproductive tactics male chose: female defence polygyny when females are clumped (interference competition), but a searching tactic when females are dispersed (scramble competition). In contrast to predictions arising from theory on scramble competition, male body mass was important in determining fitness only in the year when females were dispersed, but not in other years. 8. Our results indicate that the differentiation between conditional and mixed strategies is not an absolute one. In many other species, environmental conditions might fluctuate temporally and spatially so that the normally suboptimal tactic yields similar fitness to the (usually) dominant tactic or that only a single tactic prevails. 9. We suggest the term single strategy, independent of current fitness consequences, for systems where tactics are not genetically determined, in contrast to genetically determined alternative strategies.     

Evolutionarily [corrected] stable strategies: a review of basic theory

Widely successful in applied population biology, the Evolutionarily Stable Strategy concept remains controversial because of the severe restrictions present in its original formulation. We review theory which explores and relaxes these restrictions, finding the concept to be quite robust and adaptable, incorporating considerations such as genetics, population diversity, environmental variability, and mutation.     

Estrogen in the adult male reproductive tract: A review

Testosterone and estrogen are no longer considered male only and female only hormones. Both hormones are important in both sexes. It was known as early as the 1930's that developmental exposure to a high dose of estrogen causes malformation of the male reproductive tract, but the early formative years of reproductive biology as a discipline did not recognize the importance of estrogen in regulating the normal function of the adult male reproductive tract. In the adult testis, estrogen is synthesized by Leydig cells and the germ cells, producing a relatively high concentration in rete testis fluid. Estrogen receptors are present in the testis, efferent ductules and epididymis of most species. However, estrogen receptor-α is reported absent in the testis of a few species, including man. Estrogen receptors are abundant in the efferent ductule epithelium, where their primary function is to regulate the expression of proteins involved in fluid reabsorption. Disruption of the α-receptor, either in the knockout (αERKO) or by treatment with a pure antiestrogen, results in dilution of cauda epididymal sperm, disruption of sperm morphology, inhibition of sodium transport and subsequent water reabsorption, increased secretion of Cl^-, and eventual decreased fertility. In addition to this primary regulation of luminal fluid and ion transport, estrogen is also responsible for maintaining a differentiated epithelial morphology. Thus, we conclude that estrogen or its α-receptor is an absolute necessity for fertility in the male.     

Infanticide as an alternative male reproductive strategy in langurs: A mathematical model

This paper makes explicit some of the assumptions underlying the view that infanticide is one of two (or more) alternative reproductive strategies utilized by adult male langur monkeys (genus Presbytis). A mathematical model has been developed from these assumptions, and formulae derived which give the equilibrium proportion of infanticidal males expected in langur populations under any given set of reproductive and demographic conditions. Together with estimates of adult male reproductive success obtained from a previous analysis of langur infanticide, these formulae were then used to calculate the precise proportion of infanticidal males expected in natural populations of langurs characterized by specific average male tenures. Further, the number of generations required for such populations to reach their predicted equilibrium was estimated using a simple computer model of langur population dynamics. The present work has thus produced several quantitative predictions which are directly falsifiable with observational data obtainable from wild populations of langur monkeys. With only slight modification, the present model may also be applied to the numerous other primate and non-primate species whose mating systems include many of the same general features as that of langurs.     

Endocrine mediation of vertebrate male alternative reproductive tactics: the next generation of studies

In many species of animals, males may achieve reproductive successvia one of several alternative reproductive tactics. Over thepast decade or so, there has been a concerted effort to investigateendocrine mechanisms that underlie such discrete behavioral(and often morphological) variation. In vertebrates, the firstgeneration of studies focused on potential organizational oractivational effects of steroid hormones (Moore, 1991; Mooreet al., 1998). Some of these studies have made it clear that,in addition to circulating hormone levels, one must also considerother aspects of the endocrine system, including hormone receptors,binding globulins and potential interactions among endocrineaxes. In this paper, I review recent work on endocrine mechanismsand suggest possibilities for future investigation. I highlighthow individual variation in sensitivity to environmental conditions,particularly with respect to various stressors, may accountfor the existence of alternative male reproductive phenotypes.Along these lines, I briefly explain the logic behind our workwith male phenotypes of longear sunfish (Lepomis megalotis)that is aimed at determining the tissue-specific distributionand activity of two enzymes that are common to androgen andglucocorticoid metabolism. A major goal of our work is to examinethe potential role of steroidogenic enzymes in the transductionof environmental information to influence the expression ofalternative male reproductive phenotypes.     

Conditional male dimorphism and alternative reproductive tactics in a Neotropical arachnid (Opiliones)

In arthropods, most cases of morphological dimorphism within males are the result of a conditional evolutionarily stable strategy (ESS) with status-dependent tactics. In conditionally male-dimorphic species, the status’ distributions of male morphs often overlap, and the environmentally cued threshold model (ET) states that the degree of overlap depends on the genetic variation in the distribution of the switchpoints that determine which morph is expressed in each value of status. Here we describe male dimorphism and alternative mating behaviors in the harvestman Serracutisoma proximum. Majors express elongated second legs and use them in territorial fights; minors possess short second legs and do not fight, but rather sneak into majors’ territories and copulate with egg-guarding females. The static allometry of second legs reveals that major phenotype expression depends on body size (status), and that the switchpoint underlying the dimorphism presents a large amount of genetic variation in the population, which probably results from weak selective pressure on this trait. With a mark-recapture study, we show that major phenotype expression does not result in survival costs, which is consistent with our hypothesis that there is weak selection on the switchpoint. Finally, we demonstrate that switchpoint is independent of status distribution. In conclusion, our data support the ET model prediction that the genetic correlation between status and switchpoint is low, allowing the status distribution to evolve or to fluctuate seasonally, without any effect on the position of the mean switchpoint.     

Steroid hormones in bluegill, a species with male alternative reproductive tactics including female mimicry

The proximate mechanisms underlying the evolution and maintenance of within-sex variation in mating behaviour are still poorly understood. Species characterized by alternative reproductive tactics provide ideal opportunities to investigate such mechanisms. Bluegill (Lepomis macrochirus) are noteworthy in this regard because they exhibit two distinct cuckolder (parasitic) morphs (called sneaker and satellite) in addition to the parental males that court females. Here we confirm previous findings that spawning cuckolder and parental males have significantly different levels of testosterone and 11-ketotestosterone. We also report, for the first time, that oestradiol and cortisol levels are higher in cuckolders than in parental males. The two cuckolder morphs did not differ in average levels of any of the four hormones. However, among satellite males which mimic females in appearance and behaviour, there was a strong negative relationship between oestradiol levels and body length, a surrogate for age. This finding suggests that for satellite males, oestradiol dependency of mating behaviour decreases with increasing mating experience. Although such decreased hormone dependence of mating behaviour has been reported in other taxa, our data represent the first suggestion of the relationship in fishes.     

Tactics for male reproductive success in plants: contrasting insights of sex allocation theory and pollen presentation theory

The basic tenet of sex allocation theory is that an organism'sreproductive success, through either male or female function,can be represented as a sex-specific, monotonic, increasingfunction of the organism's investment of resources in that function.The shapes of these curves determine what patterns of resourceallocation can be evolutionarily stable. Although SA theoryhas stimulated creative thinking about plant sexual tactics,quantifying the shapes of male and female gain curves has provenso difficult that other approaches must be considered. I contrastsex allocation theory to a different, emerging viewpoint, pollenpresentation theory (PPT), which attempts to address variationin reproductive success by measuring and modeling the quantitativefates of pollen grains. Models suggest that RS through malefunction depends heavily on the packaging and gradual dispensingof pollen to pollinators, even with the amount of investmentheld constant. Many plants do deploy pollen gradually, throughmorphological and "behavioral" mechanisms that range from obviousto subtle. They may thereby influence many aspects of the evolutionof sexual modes in plants, including transitions between dioecyand cosexuality. After reviewing the main implications of themodels, I discuss recent work aimed at testing some key assumptionsand predictions by functional and comparative studies in thegenus Penstemon. Species of Penstemon conform to PPT predictionsthat bee-adapted flowers will restrict per-visit pollen availabilitymore than hummingbird-adapted flowers.     

Fish hatching strategies: a review

The paper presents differences in the distribution of hatching gland cells, and the location of egg envelope digestion, the significance of hatching movements, and the ways larvae escape from egg envelopes. A review of the literature on the hatching orientation of 34 fish species is compared. No correlation was seen between hatching orientation and egg diameter or newly hatched larva length, nor newly hatched larvae length ratio to egg diameter. Photographs of twelve freshwater species present the moment of hatching either head first or tail first. Some differences were shown in swelling between eggs incubated in commercial hatchery and developed in natural conditions, as well as possible effect of these differences on hatching.     

Alternative reproductive strategies: a queen perspective in ants

Ant colonies are commonly thought to have a stable and simple family structure, with one or a few egg-laying queens and their worker daughters. However, recent genetic studies reveal that the identity of breeding queens can vary over time within colonies. In several species, some queens are apparently specialized to enter established colonies instead of initiating a new colony on their own. The previously overlooked occurrence of queen turnover within colonies has important consequences not only on the genetic structure and nature of kin conflict within colonies, but also on the evolution of social parasitism.     

The energetic costs of alternative male reproductive strategies in <Emphasis Type="Italic">Xiphophorus nigrensis</Emphasis>

The coexistence of alternative male mating strategies depends on the balance between costs and benefits. Here we examine the short-term metabolic costs associated with distinct reproductive strategies in the genetically determined alternative male phenotypes of a northern swordtail, Xiphophorus nigrensis. In this species, large males court females, non-adorned small males chase females, and intermediate males exhibit both courtship and chase behaviors. Using intermittent flow respirometry, we measure oxygen consumption rates and behaviors of each size class in isolation and in the presence of a female. Changes in oxygen consumption between solitary and female presence trials (ΔVO₂) correlated significantly with standard length across all size classes (r = 0.42). Only the large male class exhibited a significant increase in oxygen consumption in female-present trials exhibiting a range of increase from 2 to 200% relative to solitary metabolic rates, but costs of specific courtship displays could not be demonstrated. Sword length explained 54–57% of the variation in oxygen consumption in large male solitary trials and 63–65% in the female-present trials independent of any behavioral correlation with sword length. Our results exhibit similarities to condition-dependent alternative mating systems where the female-favored phenotype has higher energetic costs.