Male Investment Research Articles

Burrow ornamentation in the fiddler crab (Uca leptodactyla): female mate choice and male–male competition

Non-biological ornamentation is found in the nests and burrows of different kinds of animals. We evaluated here whether sand hoods constructed by male fiddler crabs (Uca leptodactyla) are one of the signals used by males to attract females during courtship. We observed females when they were walking among the males, and we quantified the proportion of females that visited male burrows with and without ornamentation and the choice to stay in a male’s burrow. Females visited more burrows with hoods than burrows without hoods, and they chose significantly more builder males. Male investment in ornamentation nevertheless decreased when the proportion of females increased in the area. Male investment was not correlated with the proportion of non-builder males nearby, but was positively correlated with overall density. The density sex ratio, however, was more male-biased in high-density than in low-density areas suggesting that even if building attracts females, the function could be related to male competition for mates.

The evolution of monogamy in response to partner scarcity

The evolution of monogamy and paternal care in humans is often argued to have resulted from the needs of our expensive offspring. Recent research challenges this claim, however, contending that promiscuous male competitors and the risk of cuckoldry limit the scope for the evolution of male investment. So how did monogamy first evolve? Links between mating strategies and partner availability may offer resolution. While studies of sex roles commonly assume that optimal mating rates for males are higher, fitness payoffs to monogamy and the maintenance of a single partner can be greater when partners are rare. Thus, partner availability is increasingly recognized as a key variable structuring mating behavior. To apply these recent insights to human evolution, we model three male strategies – multiple mating, mate guarding and paternal care – in response to partner availability. Under assumed ancestral human conditions, we find that male mate guarding, rather than paternal care, drives the evolution of monogamy, as it secures a partner and ensures paternity certainty in the face of more promiscuous competitors. Accordingly, we argue that while paternal investment may be common across human societies, current patterns should not be confused with the reason pairing first evolved.

Lifetime reproductive effort is equal between the sexes in seed beetles (Callosobruchus maculatus): dispelling the myth of the cheap male

In the evolution of sexual reproduction, the development of asymmetrical gametes (anisogamy) often leads to the characterisation that males invest less in reproduction than females. This view is founded on the fact that male investment in individual gametes (sperm) and in gonadal tissue is often less than that of females. While it may be true that within a single mating interaction the relative reproductive investment by males and females differs, over their respective lifetimes an evolutionary view predicts that total lifetime reproductive investment should be the same for both sexes. We tested this prediction by measuring total reproductive investment in reproducing adult male and female seed beetles. Since seed beetle adults are facultatively aphagous, not needing to feed or drink as adults, we could track the daily loss of biomass in the reproducing adults as a proxy for total lifetime investment in maintenance and reproduction. By the end of their lifetime there was not a significant difference in total reproductive effort between males and females. Both sexes invested 70 ± 1% SE of their initial body mass in maintenance and reproduction. Altering sex ratios, creating male-biased or female-biased treatments, significantly influenced total investment between the sexes, but not in the manner predicted. Ours is one of the few studies that have measured total adult lifetime reproductive investment in an organism, and our results support the theoretical expectation of equal total reproductive investment between the sexes.

Socially cued developmental plasticity in web-building spiders.

BackgroundSocially cued anticipatory plasticity (SCAP) has been proposed as a widespread mechanism of adaptive life-history shifts in semelparous species with extreme male mating investment. Such mating systems evolved several times independently in spiders and male reproductive success should critically depend on timely maturation and rapid location of a receptive and, ideally, virgin female. We experimentally investigated socially cued anticipatory plasticity in two sympatric, closely related Nephila species that share many components of their mating systems, but differ in the degree to which male reproductive success depends on mating with virgin females. Juveniles of both species were reared either in the presence or absence of virgin female silk cues. We predicted strong selection on socially cued plasticity in N. fenestrata in which males follow a highly specialized terminal investment strategy, but expected a weaker plastic response in N. senegalensis in which males lost the ability to monopolize females.ResultsContrary to our predictions, N. fenestrata males presented with virgin female silk cues did not mature earlier than siblings reared isolated from such cues. Males in N. senegalensis, however, showed a significant response to female cues and matured several days earlier than control males. Plastic adjustment of maturation had no effect on male size.ConclusionsOur results indicate that a strong benefit of mating with virgins due to first male sperm priority does not necessarily promote socially cued anticipatory plasticity. We emphasize the bidirectional mode of developmental responses and suggest that this form of plasticity may not only yield benefits through accelerated maturation, but also by avoiding costs of precipitate maturation in the absence of female cues.

Territory Availability at Different Spatial Scales does not Affect Fighting Investment in Males of the Lycaenid Butterfly Strymon mulucha

AbstractIn territorial species, rivals investment in fights over territories may increase when the availability of suitable areas for defense is low. This should occur because low territory availability may increase the costs to maintain and acquire territories. Although such process occurs in small spatial scales (local scale), territory availability in larger scales (regional scale) may also affect fighting investment, as losers should incur additional dispersing costs to find new territories. In this study, we used males of the hilltopping butterfly Strymon mulucha to evaluate the hypothesis that males should invest more in territorial fights when the costs to find new territories are higher (both at local and at regional scale). We timed male–male contests for territories located in 12 hilltops and measured male density per territory in each hilltop (local scale). We also quantified the distance between hilltops containing suitable areas for territories (regional scale). Male–male contests lasted 21 s on average, and copulations did not occur during the observations. The duration of contests was unrelated to the male density per territory or to the distance among hilltops, indicating that the investment in fights was unaffected by the availability of territorial sites, independent of the spatial scale. As male–male contests in S. mulucha are longer than the mean contest duration in other butterfly species and mating is extremely rare, we suggest that the value of each territory may be high enough to favor males that always invest as much as possible in contests.

Beyond LARC: Advancing Reproductive Health to Include Men.

The authors argue that men should be involved in the reproductive health discourse. They express concern over the lack of inclusion of men in the discussion about the long-acting reversible contraceptives (LARC) technology and discuss topics including enhancing the role of partners in reproduction, the potential benefits of men's participation in reproductive health education, and male investment in childbearing and rearing.

Sexual cannibalism increases male material investment in offspring: quantifying terminal reproductive effort in a praying mantis.

Models of the evolution of sexual cannibalism argue that males may offset the cost of cannibalism if components of the male body are directly allocated to the eggs that they fertilize. We tested this idea in the praying mantid Tenodera sinensis Males and females were fed differently radiolabelled crickets and allowed to mate. Half of the pairs progressed to sexual cannibalism and we prevented cannibalism in the other half. We assess the relative allocation of both male-derived somatic materials and ejaculate materials into the eggs and soma of the female. Our results show that male somatic investment contributes to production of offspring. The eggs and reproductive tissues of cannibalistic females contained significantly more male-derived amino acids than those of non-cannibalistic females, and there was an increase in the number of eggs produced subsequent to sexual cannibalism. Sexual cannibalism thus increases male material investment in offspring. We also show that males provide substantial investment via the ejaculate, with males passing about 25% of their radiolabelled amino acids to females via the ejaculate even in the absence of cannibalism.

Experimental evolution under hyper-promiscuity in Drosophila melanogaster.

BackgroundThe number of partners that individuals mate with over their lifetime is a defining feature of mating systems, and variation in mate number is thought to be a major driver of sexual evolution. Although previous research has investigated the evolutionary consequences of reductions in the number of mates, we know little about the costs and benefits of increased numbers of mates. Here, we use a genetic manipulation of mating frequency in Drosophila melanogaster to create a novel, highly promiscuous mating system. We generated D. melanogaster populations in which flies were deficient for the sex peptide receptor (SPR) gene – resulting in SPR- females that mated more frequently – and genetically-matched control populations, and allowed them to evolve for 55 generations. At several time-points during this experimental evolution, we assayed behavioural, morphological and transcriptional reproductive phenotypes expected to evolve in response to increased population mating frequencies.ResultsWe found that males from the high mating frequency SPR- populations evolved decreased ability to inhibit the receptivity of their mates and decreased copulation duration, in line with predictions of decreased per-mating investment with increased sperm competition. Unexpectedly, SPR- population males also evolved weakly increased sex peptide (SP) gene expression. Males from SPR- populations initially (i.e., before experimental evolution) exhibited more frequent courtship and faster time until mating relative to controls, but over evolutionary time these differences diminished or reversed.ConclusionsIn response to experimentally increased mating frequency, SPR- males evolved behavioural responses consistent with decreased male post-copulatory investment at each mating and decreased overall pre-copulatory performance. The trend towards increased SP gene expression might plausibly relate to functional differences in the two domains of the SP protein. Our study highlights the utility of genetic manipulations of animal social and sexual environments coupled with experimental evolution.Electronic supplementary materialThe online version of this article (doi:10.1186/s12862-016-0699-8) contains supplementary material, which is available to authorized users.

Male-biased sex ratio does not promote increased sperm competitiveness in the seed beetle, Callosobruchus maculatus.

Sperm competition risk and intensity can select for adaptations that increase male fertilisation success. Evolutionary responses are examined typically by generating increased strength of sexual selection via direct manipulation of female mating rates (by enforcing monandry or polyandry) or by alteration of adult sex ratios. Despite being a model species for sexual selection research, the effect of sexual selection intensity via adult sex-ratio manipulation on male investment strategies has not been investigated in the seed beetle, Callosobruchus maculatus. We imposed 32 generations of experimental evolution on 10 populations of beetles by manipulating adult sex ratio. Contrary to predictions, males evolving in male-biased populations did not increase their testes and accessory gland size. This absence of divergence in ejaculate investment was also reflected in the fact that males from male-biased populations were not more successful in either preventing females from remating, or in competing directly for fertilisations. These populations already demonstrate divergence in mating behaviour and immunity, suggesting sufficient generations have passed to allow divergence in physiological and behavioural traits. We propose several explanations for the absence of divergence in sperm competitiveness among our populations and the pitfalls of using sex ratio manipulation to assess evolutionary responses to sexual selection intensity.

Badge Size Reflects Sperm Oxidative Status within Social Groups in the House Sparrow Passer domesticus

The phenotype-linked fertility hypothesis proposes that male ornaments reflect male fertility. Male ornaments could honestly signal sperm quality due to the high susceptibility of sperm to free radicals on the one hand and the negative impact of oxidative stress on ornament elaboration on the other hand. Thus, only males with superior antioxidant defences could bear the cost of more elaborated sexual ornaments without suffering adverse fitness costs. Yet, in species where males experience differential access to fertile females, a trade-off emerges between investing into traits favouring mating opportunities (e.g. secondary sexual ornaments, social dominance, mate-guarding behaviours, etc.) or into traits favouring sperm competitive ability (e.g. sperm numbers and quality). When male sexual ornaments promote greater access to fertile females, a negative relationship can then be predicted between ornamentation and sperm quality. We tested the latter hypothesis and the phenotype-linked fertility hypothesis in wild House Sparrows Passer domesticus by exploring the relationships between sperm quality, melanin-based ornamentation, and redox status in blood and sperm. We found no correlation between badge size and sperm swimming performance. However, we found that within a social group, large-badged males better protect their ejaculates from oxidative stress, and thus produce less oxidized ejaculates. Additionally, we found that badge size did not reflect social dominance, and thus the protection of the ejaculate is independent of males’ ability to monopolize resources. Our results suggest that badge size might reflect male investment into the antioxidant protection of their sperm relative to a given social environment, and thus females may accrue both direct and indirect benefits by mating with large-badged males producing less oxidized ejaculates.

Altitude underlies variation in the mating system, somatic condition, and investment in reproductive traits in male Asian grass frogs (Fejervarya limnocharis)

There is substantial comparative and growing experimental evidence that the competition for fertilization among sperm from different males can drive variation in male reproductive investments. However, less is known about the extent of natural variation in these investments relative to environmental variables affecting resource availability and mating system dynamics, which would allow insights into the mechanisms shaping reproductive allocation. Here, we studied interpopulation variation in male investments in testis size and sperm length across 25 populations of the Asian grass frog Fejervarya limnocharis along a 1550-km latitudinal and 1403-m altitudinal transect in China. We found relative testis mass and sperm length, male somatic condition, and the male/female sex ratio to increase with elevation but not latitude or longitude. Our results suggest that environmental variation may underlie local adaptations to reproductive investments among natural populations, mediated by differences in the availability of both resources and sexual partners (including the resulting male–male competition). These findings contrast with previous predictions that increasing latitude and/or elevation should lead to declining reproductive investments in male anurans due to shortening breeding seasons, declining resource availability, and lowering (rather than increasing) male/female sex ratios. We discuss these species differences in the context of differential resource allocation strategies, breeding ecology, and patterns of male–male competition. These differences show the need for future work on reproductive investments in anurans beyond the few model systems and for potential extension of the theoretical framework to species with different mating systems and strategies. Despite a broad theoretical framework of how environmental parameters can shape mating systems and these, in turn, drive the evolution of reproductive traits, there is limited empirical evidence from natural populations. We examined differences in the size of testes and sperm between males between natural populations along latitudinal and altitudinal transects. We found that at high elevation, males were relatively heavier and had longer sperm and disproportionately large testes, and the sex ratio was more male-biased. These interpopulation differences may reflect local adaptations to variation in the resource availability and temporal patterns of female availability, which affects the breeding synchrony, sperm demand, and male–male competition for mates and paternity. However, our results differ from previous studies of frogs, possibly due to different breeding ecology, which highlights the need for further work and potential extension of theoretical predictions to non-model anurans.

Increased population density reduces body growth and female investment in a simultaneous hermaphrodite.

Sex allocation theory applied to hermaphrodites assumes that there is a trade off between the allocation of resources to male and female functions, within a fixed reproductive resource budget. Charnov's classic resource allocation model predicts a more female-biased sex allocation when competition among different sperm donors is low due to diminishing fitness returns for male investment. By manipulating the social group size, one automatically changes the population density at which individuals live. Increasing population density may affect reproductive allocation, leading to resource competition and/or to increased concentration of harmful metabolites. This could lead to an over- or underestimation of the individual adjustment of sex allocation responses to mating opportunities. In this article, we tested the effects of density and social group size separately on female investment and body growth (considered as proxy of the overall energy budget) in the simultaneously hermaphroditic polychaete worm Ophryotrocha diadema. We manipulated social group size (i.e., monogamous and promiscuous regimes) and density (i.e., 4 levels) using a full-factorial design, to identify the underlying factor affecting female allocation (in terms of egg production) and body growth. In contrast to findings of previous experiments, we found that an increase in population density reduced body growth and egg production of hermaphrodites irrespective of social group size. We advance the hypothesis that the increase of catabolites and oxygen consumption in high-density conditions reduces the overall resource budget and this could obscure group size effects on female fecundity.

Direct benefits from choosing a virgin male in the European grapevine moth, Lobesia botrana

In Lepidoptera, male investment in the ejaculate usually declines over consecutive matings, a depletion that could have profound consequences for female reproductive output. Since successive matings can affect the ability of males to provide phenotypic benefits, there may be strong selection for females to discriminate between males with different mating experience. The aim of our study was to determine whether monandrous females of the European grapevine moth, Lobesia botrana , are able to discriminate between males of different quality based on their mating experience in order to maximize direct benefits (by receiving large spermatophores from virgin males) and minimize mating costs (by avoiding low-quality nonvirgin males). Nonvirgin males produced spermatophores five times smaller than those of virgin males; consequently, mating with nonvirgin males significantly reduced female fecundity and increased their motivation to remate. In a mate preference experiment, we found that females were more likely to mate with virgin males and more frequently rejected nonvirgin mates. Moreover, nonvirgin males required more time to achieve mating than virgin males. Our results suggest that females are able to discriminate between males with different mating experience, and prefer virgin males, thereby maximizing direct benefits associated with receiving large spermatophores.

Reproductive strategy of the invasive sharpbelly,Hemiculter leucisculus(Basilewsky 1855), in Erhai Lake, China

This study describes the reproductive strategy of the sharpbelly Hemiculter leucisculus, an invasive and dominant species in Erhai Lake in China with the goal of understanding how reproductive strategy contributes to its environmental adaptability and invasive potential. Specimens (n = 3583) were collected monthly or bimonthly from July 2009 to June 2011 (min: 114-Feb, max: 883-Aug), using gill nets (inner/outer mesh = 30/110 mm, stretched mesh). Gonads were removed, weighed and preserved for further (histological) analyses. Oocyte size-frequency distribution was continuous and had advanced vitellogenic oocytes with postovulatory follicles present in spawning females, both suggesting that sharpbelly is a multiple spawner with adhesive eggs. Spawning extended from April to September, with the peak period from May to August. Standard lengths (SL, cm) at minimal observed maturity/L50/L99.9 values were 4.6/5.6/10.5 for females and 5.1/5.5/7.5 cm for males, respectively. Females were over-represented (P < 0.01) in SL-classes over 9 cm and males completely absent from the 13 to 19 cm SL-classes. Overall sex ratio was highly significantly (P < 0.01) biased towards females (♀ = 1518, ♂ = 685, ♀/♂ = 2.21), however this was reversed in the spawning stock (8.3–16 cm, ♀ = 58, ♂ = 142, ♂/♀ = 2.45, P < 0.01). Batch spawning, a long spawning period, high male investment in reproduction and adhesive eggs all represent local adaptations in reproductive strategy that, along with other environmental factors, contribute to the invasion success of sharpbelly in Erhai.

Prolonged copulations as an alternative to male nuptial gift investment in the bushcricket Letana inflata (Orthoptera: Tettigoniidae)

In most bushcricket species, the male transfers a nuptial gift to the female during mating, consisting of a gelatinous spermatophylax attached to the paired ampulla with the sperm. The spermatophylax acts as a sperm protection device; during its consumption, the sperm are transferred into the female’s spermatheca. Males of the bushcricket Letana inflata (Brunner von Wattenwyl, 1878) show strongly extended copulation duration. When the pair finally separates, only an ampulla is visible at the females’ genital opening, but no spermatophylax. To better understand copulation dynamics in the absence of a spermatophylax, we studied copula duration and sperm transfer pattern. Our results show that in Letana inflata the missing spermatophylax is replaced by extended copulation, securing the transfer of sperm into the spermatheca.

The influence of recent social experience and physical environment on courtship and male aggression.

BackgroundSocial and environmental factors can profoundly impact an individual’s investment of resources into different components of reproduction. Such allocation trade-offs are expected to be amplified under challenging environmental conditions. To test these predictions, we used a desert-dwelling fish, the desert goby, Chlamydogobius eremius, to experimentally investigate the effects of prior social experience (with either a male or a female) on male investment in courtship and aggression under physiologically benign and challenging conditions (i.e., low versus high salinity).ResultsWe found that males maintained a higher level of aggression towards a rival after a recent encounter with a female, compared to an encounter with a male, under low (but not high) salinity. In contrast, male investment in courtship behaviour was unaffected by either salinity or social experience.ConclusionTogether, our results suggest that male investment in aggression and courtship displays can differ in their sensitivity to environmental conditions and that not all reproductive behaviours are similarly influenced by the same environmental context.

Nest as an extended phenotype signal of female quality in the great reed warbler

Extended phenotypes with signalling function are mostly restricted to animal taxa that use construction behaviour during courtship displays. However, they can be used also as post‐mating signals of mate quality, allowing individuals to obtain reliable information about their partners. Nest size may have such a signalling function and a lot of indirect evidence supports this view. However, direct evidence based on an experimental approach is still widely missing. Here we test the role of nest size in post‐mating signalling of mate quality in the great reed warbler Acrocephalus arundinaceus, a passerine with female‐restricted nest‐building behaviour. Based on observational data, clutch size, nestling weight, brood size and fledglings’ propensity to return to their natal site positively correlated with nest size. Moreover, we experimentally enlarged great reed warbler nests to investigate whether this manipulation affects male investment in feeding. We found that males fed their nestlings significantly more intensively on enlarged nests than those on control nests. This suggests that nest size in this species serves as a signal of female quality or willingness to invest in reproduction and that it pays males to enhance their feeding effort according to this signal. Thus, we provide convincing evidence that animal communication takes place through the extended phenotypes and that post‐mating signalling of quality is not restricted only to males, but may function equally well in females.

Context‐ and State‐Dependent Male Mate Choice in a Sexually Cannibalistic Spider

AbstractHigh male mating investment may favor selection on male mate choice particularly if females vary in quality. Terminal investment strategies constitute a maximal mating effort and have evolved independently in the absence of paternal investment in several spider taxa including the genus Argiope. To test for male mate preferences in the above context, we used the sexually cannibalistic spider A. bruennichi. We varied male state (mating status and post‐maturation age) as well as the competitive context and quantified male mate choice decisions between females of different states and developmental stages in binary choice tests. We found an overall adaptive preference for the virgin against the mated female regardless of male mating state. Furthermore, we demonstrated that older males paid more attention to female fecundity‐related traits than to mating status. In a second set of experiments, we offered males a choice between a virgin and a subadult female and varied the competitive context which had no effect on male decisions. Curiously, a preference for the virgin adult female was only apparent after exclusion of females that matured &lt;3 d prior to the test. Repeated tests of males supported the hypothesis that males do not distinguish between a freshly matured virgin female and a subadult female. Our results show that male spiders execute mate choice based on information collected from female silk strands and that they integrate their own state into mating decisions.

When should male squid prudently invest sperm?

Ejaculate production can be costly and males are expected to prudently allocate this potentially limiting resource to higher quality females. However, relatively little is known about facultative sperm allocation in response to the quality distribution of sequentially encountered females, despite this being a more realistic scenario for males in many species. Here, we examined patterns of male investment in a squid, Sepiadarium austrinum, when presented sequentially with small versus large females. Owing to a positive size – fecundity relationship in this species, large and small females are expected to differ in terms of their perceived quality to males as potential mating partners. Yet, despite large sperm investment and significant variation in female quality, sperm investment was determined only by mating order, with males consistently decreasing sperm investment in second matings. These results highlight that, when mates are encountered sequentially rather than simultaneously, prudent sperm allocation may not occur when it is otherwise predicted.

Altitudinal variation in male reproductive investment in a polyandrous frog species (Hyla gongshanensis jingdongensis)

Competition for fertilization in multi-male group spawning can drive variation in male reproductive investment (i.e., testis mass and sperm size). Inter-population comparisons of variation in energetic availability and allocation along geographical gradients allow insights into the mechanisms shaping the reproductive investments of animals. Although inter-population differences in female reproductive investment (i.e., clutch size and egg size) have been studied extensively across a wide range of taxa, little information on variation in reproductive investment in males is available. Here, we studied altitudinal variation in testis mass and sperm length among three populations in the Jingdong tree frog (Hyla gongshanensis jingdongensis), a polyandrous species, in Yunnan Province in China. The results showed that individuals exhibited smaller testes at higher altitudes while testes mass was positively correlated with body size, body condition and age. Longer sperm length was observed in the middle-altitude population. Moreover, we found that sperm number was positively correlated with testes mass and sperm length. Our correlational findings suggest that environmental constraints at high altitude select for less investment in testes and offspring number.