Male Reproductive Investment Research Articles

Emergence of games from ecological trade-offs: longevity changes strategies for extra-pair mating in birds

Each member of a breeding pair benefits if the other does more of the parental investment, so there is scope for behaviours that can be interpreted as both cooperative and competitive games between males and females. Extra-pair mating, widespread among socially monogamous birds, adds extra conflict but also potential opportunity to these social interactions. We analyse an individual-based model of a social environment with simple behavioural strategies where game-like patterns and cooperative outcomes emerge. The model focuses on three evolving traits: female propensity for extra-pair copulations and male investment in territorial behaviour and care. Male traits are reaction norms that use experienced within and extra-pair copulations as information input. We found that female extra-pair mating provided incentives for males to reduce territorial aggression and increase care for offspring. However, when adult survival was higher, male investment in care and territoriality changed from being negatively to positively correlated. This happened because longer life expectancy gave more behavioural opportunities for males, where nest desertion maximises lifetime male fitness when female extra-pair copulation is high. This outcome evolved gradually, with stable periods of intermediate extra-pair mating and low territoriality. These were punctuated by cycles of high extra-pair mating, nest desertion, reduced extra-pair mating and relapse to aggressive territoriality before a new stable phase was established. Each successive trait cycle was faster and smaller, indicating that through evolution of reaction norms, the gene pool has a long history that canalizes the evolution of behaviours, which can be interpreted as emergence and refinement of frequency-dependent games.Significance statementMost birds that mate in monogamous pairs engage in extra-pair copulations. Males of some species invest (in varying proportions) in offspring that are genetically related only to their social female. The great variability of extra-pair mating levels among different species and populations, supported by numerous field studies, indicates that social and ecological factors play a crucial role in shaping the behaviour. We analyse a computer model in which extra-pair mating evolves concurrently with male reproductive investments in territory defence and offspring care and show how common ecological trade-offs may change the social dynamics within a breeding population and lead to the emergence of complex social interactions between males, females and their neighbours.

An evolutionary explanation of female-biased sexual size dimorphism in North Sea plaice, Pleuronectes platessa L.

Sexual size dimorphism (SSD) is caused by differences in selection pressures and life-history trade-offs faced by males and females. Proximate causes of SSD may involve sex-specific mortality, energy acquisition, and energy expenditure for maintenance, reproductive tissues, and reproductive behavior. Using a quantitative, individual-based, eco-genetic model parameterized for North Sea plaice, we explore the importance of these mechanisms for female-biased SSD, under which males are smaller and reach sexual maturity earlier than females (common among fish, but also arising in arthropods and mammals). We consider two mechanisms potentially serving as ultimate causes: (a) Male investments in male reproductive behavior might evolve to detract energy resources that would otherwise be available for somatic growth, and (b) diminishing returns on male reproductive investments might evolve to reduce energy acquisition. In general, both of these can bring about smaller male body sizes. We report the following findings. First, higher investments in male reproductive behavior alone cannot explain the North Sea plaice SSD. This is because such higher reproductive investments require increased energy acquisition, which would cause a delay in maturation, leading to male-biased SSD contrary to observations. When accounting for the observed differential (lower) male mortality, maturation is postponed even further, leading to even larger males. Second, diminishing returns on male reproductive investments alone can qualitatively account for the North Sea plaice SSD, even though the quantitative match is imperfect. Third, both mechanisms can be reconciled with, and thus provide a mechanistic basis for, the previously advanced Ghiselin-Reiss hypothesis, according to which smaller males will evolve if their reproductive success is dominated by scramble competition for fertilizing females, as males would consequently invest more in reproduction than growth, potentially implying lower survival rates, and thus relaxing male-male competition. Fourth, a good quantitative fit with the North Sea plaice SSD is achieved by combining both mechanisms while accounting for sex-specific costs males incur during their spawning season. Fifth, evolution caused by fishing is likely to have modified the North Sea plaice SSD.

Sex‐specific breeding phenologies in the North American deer mouse (Peromyscus maniculatus)

AbstractEffects of global climate change on population persistence are often mediated by life‐history traits of individuals, especially the timing of somatic growth, reproductive development, and reproduction itself. These traits can vary among age groups and between the sexes, a result of differential life‐history tactics and levels of lifetime reproductive investment. Unfortunately, the trait data necessary for revealing sex‐specific breeding behaviors and use of breeding cues over reasonably large geographic areas remain sparse for most taxa. In this study, we assembled and analyzed a new reproductive trait base for the North American deer mouse (Peromyscus maniculatus) from digitized natural history specimens and field censuses. We used the data to reconstruct sex‐specific breeding phenologies and their drivers within and among North American ecoregions. Male and female phenologies varied across the geographic range of this species, with discordance in timing and intensity being highest in regions of lower seasonality (and longer breeding seasons). Reliance on environmental variables as breeding cues also appeared to vary in a sex‐specific manner, being most similar for photoperiod and least similar for temperature (positive male response and negative female response); in addition, model validation indicated that phenological models generalized better for males than for females. Finally, our individual‐level trait data also show that male reproductive investment (quantified as relative testis size) varies across the vastly different abiotic and social (i.e., female breeding) contexts studied here. By harmonizing across a broad set of digital data resources, we demonstrate the potential to uncover drivers of phenological variation within species and inform global change predictions at multiple scales of biological organization.

Consequences of the Reproductive Effort of Dioecious Taxus baccata L. Females in a Generative Bud Removal Experiment-Important Role of Nitrogen in Female Reproduction.

Dioecious species differ in the pattern and intensity of male and female reproductive investments. We aimed to determine whether female shoots deprived of generative buds show biochemical features, indicating their less-pronounced reproductive effort. For this purpose, the same branches of mature Taxus baccata females were deprived of generative organs. In the second and third years of the experiment, measurements were made in every season from the control and bud-removed shoots of females and control males. Bud removal caused an increase in nitrogen concentration almost to the level detected in the needles of male specimens, but only in current-year needles. Moreover, differences between male and control female shoots were present in the C:N ratio and increment biomass, but they disappeared when bud removal was applied to females. Additionally, between-sex differences were observed for content of phenolic compounds, carbon and starch, and SLA, independent of the female shoot reproductive effort. The study revealed that nitrogen uptake in seeds and arils may explain the lower nitrogen level and consequently the lower growth rate of females compared to males. At the same time, reproduction did not disturb carbon level in adjacent tissues, and two hypotheses explaining this phenomenon have been put forward.

Testis Size Variation and Its Environmental Correlates in Andrew's Toad (Bufo andrewsi).

Reproductive investments influenced by environmental conditions vary extensively among geographically distinct populations. However, investigations of patterns of intraspecific variation in male reproductive investments and the mechanisms shaping this variation in anurans remain scarce. Here, we focused on the variation in testis size in 14 populations of the Andrew's toad Bufo andrewsi, a species with weak dispersal ability but wide distribution in southwestern China, to establish whether male reproductive investment varies on an environmental gradient. Our analysis revealed a significant variation in relative testis size across populations, and a positive correlation between testis size and body condition. We, however, found no geographic trends explaining the variability in the testis size. The relative testis size did not increase with increasing latitude or altitude. We also found no relationship between relative testis size and rainfall, but a negative correlation with the coefficient of variation of temperature, with larger testes under stable environments. These findings suggest that the decreased male reproductive investment of this species may be a consequence of harsher or fluctuating environmental conditions.

How does access to water at different life-stages affect male investment in reproduction and survival?

Holometabolous insects have four distinct life-stages – eggs, larvae, pupae and adults. Active resource acquisition generally occurs during either or both the larval and adult stages. Previous research on the acquisition of food resources in holometabolous insects, has shown that resources acquired during each of these life-stages can differ in how they are allocated to different traits, and how they affect fitness. In addition to food, water is also an essential resource needed for a range of biological processes that enhance fitness. Yet, how water acquired at different life-stages affects key fitness traits is still not clear. Here, we manipulated both developmental and adult water availability of male seed beetles (Callosobruchus maculatus) to explore how water acquired at each life-stage affects a range of fitness related traits, including body mass, ejaculate weight, mating behavior and lifespan. Our results indicate that the juvenile environment had little effect on body weight, ejaculate weight, ejaculate replenishment or lifespan, but did influence male mating behavior in both early and late adult life. This contrasts with the adult environment, which had strong effects on weight loss, ejaculate size and lifespan but little effect on mating behavior. Males with access to water during adulthood transferred larger ejaculates during their first mating, lost less weight as they aged, and lived longer. These results suggest that water acquired during development and adulthood are allocated differently to a variety of fitness traits across life.

Influence of the lunar cycle and spatial gradients on size-dependent male and female reproductive investment decisions of a protogynous reef fish

Coral reef fish species experience variable environments and may employ a range of reproductive strategies to help them maximize fitness. Here, we explore patterns of variation in size- and sex-dependent spawning strategies (pair spawning, group spawning, and streaking tactics) of a sex-changing, highly iteroparous fish (the sixbar wrasse Thalassoma hardwicke) across the lunar month, and in relation to proximity to the reef edge. We test the hypothesis that adults vary their investment strategies as a function of body size. We evaluated reproductive behaviour patterns at 2–3 days intervals over 5 consecutive months, and found that frequencies of pair spawning, group spawning, and streaking attempts all significantly increased around the new moon and were greatest in the most exposed territories (i.e., those located closest to the reef edge). Smaller females and IP males largely curtailed reproductive activities during the full moon and third quarter moon, while larger individuals reproduced more consistently across the lunar month. Size-dependent reproductive decisions appeared to mediate frequencies of specific reproductive tactics (e.g., prevalence of pair spawning, group spawning, and streaking strategies). We speculate that (1) optimal tactics are shaped by size- and sex-dependent trade-offs between reproduction and growth in relation to environmental conditions, and that (2) individual investment decisions determine the prevailing reproductive mode at a spawning site. Variation in female choice might thereby act as a mechanism for maintaining these two reproductive modes (pair spawning and group spawning) in a population.

Experimental evolution under varying sex ratio and nutrient availability modulates male mating success in Drosophila melanogaster.

Biased population sex ratios can alter optimal male mating strategies, and allocation to reproductive traits depends on nutrient availability. However, there is little information on how nutrition interacts with sex ratio to influence the evolution of pre-copulatory and post-copulatory traits separately. To address this omission, we test how male mating success and reproductive investment evolve under varying sex ratios and adult diet in Drosophila melanogaster, using experimental evolution. We found that sex ratio and nutrient availability interacted to determine male pre-copulatory performance. Males from female-biased populations were slow to mate when they evolved under protein restriction. By contrast, we found direct and non-interacting effects of sex ratio and nutrient availability on post-copulatory success. Males that evolved under protein restriction were relatively poor at suppressing female remating. Males that evolved under equal sex ratios fathered more offspring and were better at supressing female remating, relative to males from male-biased or female-biased populations. These results support the idea that sex ratios and nutrition interact to determine the evolution of pre-copulatory mating traits, but independently influence the evolution of post-copulatory traits.

Impact of starvation on paternal reproductive investment in Neoseiulus californicus.

Neoseiulus californicus is an important biological control agent of small arthropod pests, widely used in preventive releases at low prey densities. Therefore, it is important to study reproductive investment of this species, both females and males, under environmental pressure of limited prey availability. Laboratory experiments were performed to investigate N. californicus male reproductive investment after short-time fasting or long-term starvation. When fasted for 36h, males are still able to complete a single mating with no significant change in reproductive parameters of its mate. But the total mating duration became 24% longer, especially timing for the male to fill the first spermatheca of its mate increased by 35%. If daily food availability was less than 20% of demand, males were still able to mate until the end of life, but their fertility reduced after ca. the seventh mating. Mating of some males at the end of their lives are invalid, with their mates failing to oviposit. Overall, we summarized that reproductive investment demand for a single mating was low in N. californicus males, but its priority in energy allocation was high. When starved, males tried to guarantee their mating capability, but their fertility decreased gradually.

Correction to: Anthropogenic noise reduces male reproductive investment in an acoustically signaling insect

Correction to: Anthropogenic noise reduces male reproductive investment in an acoustically signaling insect

Male ant reproductive investment in a seasonal wet tropical forest: Consequences of future climate change.

Tropical forests sustain many ant species whose mating events often involve conspicuous flying swarms of winged gynes and males. The success of these reproductive flights depends on environmental variables and determines the maintenance of local ant diversity. However, we lack a strong understanding of the role of environmental variables in shaping the phenology of these flights. Using a combination of community-level analyses and a time-series model on male abundance, we studied male ant phenology in a seasonally wet lowland rainforest in the Panama Canal. The male flights of 161 ant species, sampled with 10 Malaise traps during 58 consecutive weeks (from August 2014 to September 2015), varied widely in number (mean = 9.8 weeks, median = 4, range = 1 to 58). Those species abundant enough for analysis (n = 97) flew mainly towards the end of the dry season and at the start of the rainy season. While litterfall, rain, temperature, and air humidity explained community composition, the time-series model estimators elucidated more complex patterns of reproductive investment across the entire year. For example, male abundance increased in weeks when maximum daily temperature increased and in wet weeks during the dry season. On the contrary, male abundance decreased in periods when rain receded (e.g., at the start of the dry season), in periods when rain fell daily (e.g., right after the beginning of the wet season), or when there was an increase in the short-term rate of litterfall (e.g., at the end of the dry season). Together, these results suggest that the BCI ant community is adapted to the dry/wet transition as the best timing of reproductive investment. We hypothesize that current climate change scenarios for tropical regions with higher average temperature, but lower rainfall, may generate phenological mismatches between reproductive flights and the adequate conditions needed for a successful start of the colony.

Sex biased effect of acute heat shock on the antioxidant system of non-native round goby Neogobius melanostomus.

Monitoring oxidative stress biomarkers has become a powerful and common tool to estimate organismal condition and response to endogenous and environmental factors. In the present study, we used round goby (Neogobius melanostomus) from non-native European populations, as a model species to test sex differences in oxidative stress biomarkers. Considering sex differences in reproductive investment, we hypothesized that males would display lower resistance to abiotic stress. Fish were exposed to a heat shock (temperature elevated by 10°C) for 1h, 6h, and 12h and catalase activity (CAT), reduced glutathione (GSH), total antioxidant capacity (TAC) and lipid peroxidation (LPO) were measured in liver and muscle tissues. Liver of males was significantly more responsive compared to liver of females in all tested parameters. GSH was found to be the most responsive to heat stress exposure in both sexes. The results supported our hypothesis that male reproductive investment (territoriality, courtship, and brood care) and likelihood of only a single spawning period in their lifetime influenced on higher sensitivity of their antioxidant defence. On the other hand, for females antioxidant defence is considered more important to survive the environmental changes and successfully reproduce in the next season. Our experiments exposed fish to acute thermal stress. Further research should determine the effects of exposure to chronic thermal stress to corroborate our understanding on sex differences in antioxidant defence in the round goby.

Brain size evolution in small mammals: test of the expensive tissue hypothesis

Abstract Brain size exhibits significant changes within and between species. Evolution of large brains can be explained by the need to improve cognitive ability for processing more information in changing environments. However, brains are among the most energetically expensive organs. Enlarged brains can impose energetic demands that limit brain size evolution. The expensive tissue hypothesis (ETH) states that a decrease in the size of another expensive tissue, such as the gut, should compensate for the cost of a large brain. We studied the interplay between energetic limitations and brain size evolution in small mammals using phylogenetically generalized least squares (PGLS) regression analysis. Brain mass was not correlated with the length of the digestive tract in 37 species of small mammals after correcting for phylogenetic relationships and body size effects. We further found that the evolution of a large brain was not accompanied by a decrease in male reproductive investments into testes mass and in female reproductive investment into offspring number. The evolution of brain size in small mammals is inconsistent with the prediction of the ETH.

Seasonal change in male reproductive investment of a fish

Many animals are sexually dimorphic, whereby males may display brighter body coloration and more distinctive ornamentation than females. Fishes in temperate regions markedly change their energy allocation toward reproduction in response to the seasonal environment. Seasonal change in reproductive investment affects the expression of sexually dimorphic traits in males through gonadal weight change. Here, we report seasonal changes in body size, testis weight and sexual dimorphism of the fins (anal fin length and dorsal fin length) in the northern medaka Oryzias sakaizumii. Fish were collected periodically from a wild population (Aomori). Gonad weight increased from May to July in both males and females, corresponding to the reproductive season. Moreover, during this period, the degree of sexual dimorphism in fin length increased. To investigate the relationship between testis weight and individual differences in male fin length, we analyzed relationships among morphological traits using structural equation modeling. In the reproductive season, increased testis weight was associated with longer fin length in males, but the relationship disappeared after the reproductive season. These observations suggest that the sexually dimorphic fin in this fish is a mating signal. Results from a mating experiment also support this view. Males with larger size and/or longer fin attracted more mates than those with smaller fins, suggesting that sexual selection operates through females choosing to mate with males having longer fins.

Temporal shifts in ostracode sexual dimorphism from the Late Cretaceous to the late Eocene of the U.S. Coastal Plain

Ostracodes of the superfamily Cytheroidea exhibit sexual dimorphism in the carapace such that males are more elongate than females. This sex difference is attributed to the need of the carapace to accommodate the large male copulatory apparatus, and the degree of dimorphism is an indication of male investment in reproduction. In this study, we examine trends in sexual dimorphism, as a proxy for sexual selection, from the Late Cretaceous to the late Eocene to better understand the long-term effects of the Cretaceous/Paleogene mass extinction. We used mixture models to identify sex clusters from digitized outlines of photographed specimens and estimated size and shape dimorphism as the difference in the mean log area and the mean log length-to-height ratio for male and female clusters. We found dimorphism exhibits a phylogenetic signal; families and genera tend to occupy various restricted subsets of dimorphism space. Previous work documented that the mean and variance in size and shape dimorphism decreased sharply at the Cretaceous/Paleogene boundary, and here we show that this fauna only partially returns to Cretaceous dimorphism patterns by the late Eocene. Most surprisingly, species with both high size and shape dimorphism, which occurred in a diverse set of taxa before the extinction, remain rare into the late Eocene. These trends suggest sexual selection may respond to several possible demographic and environmental factors, which warrant further investigation.

Males can’t afford to be choosy: Male reproductive investment does not influence preference for female size in Limia (Poeciliidae)

Reproductive investment was initially thought to be the key selective force behind male mate preference for female characters, like size or ornamentation (i.e., the preference by males for certain females). Yet, evidence of polygynous species, where male reproductive investments are often inexpensive compared to those of females, have also been described to possess male preference. Our study aims to understand how reproductive investment influences the selection of choosy males in polygynous systems using two species of livebearing fishes varying in reproductive investment: Limia perugiae, in which males invest heavily into reproduction, and L. zonata in which males invest minimally into reproduction. We hypothesized that male reproductive investment when combined with fecundity selection will favour the evolution of male mate preference and thereby lead to males that invest heavily into reproduction being choosier than males that invest minimally. When male Limia were exposed to two females simultaneously, one from the small size class and one from the large size class, L. zonata chose large females over small ones, whereas L. perugiae allocated the same amount of time regardless of female size class. Although we fail to find support for our original hypotheses, our study highlights the need for a more thorough examination of non-model species like Limia. We suggest future studies analyse reproductive investment as it interacts with cryptic choice, multiple sensory cues as well as expand comparisons to multiple Limia species, especially those endemic to Cuba, Grand Cayman, and Jamaica.

Divergence of responses to variable socio‐sexual environments in laboratory populations of Drosophila melanogaster evolving under altered operational sex ratios

Post-copulatory sexual selection (PSS) is an important selective force that determines fitness in polyandrous species. PSS can be intense in some cases and can drive the evolution of remarkable ejaculate properties. In males, investment in ejaculate plays an important role in the outcome of PSS. Thus, males are expected to adaptively tailor their ejaculate according to the perceived competition in their vicinity. Plastic responses in ejaculate investment to variation in intrasexual competition are disparate and widespread in males. We investigated the evolution of plasticity in reproductive traits using Drosophila melanogaster populations evolving for more than 150 generations under male- or female-biased sex ratios. When exposed to different numbers of competitors early in their life, males from these two regimes responded differently in terms of their copulation duration and sperm competitive ability. In addition, the effect of this early life experience wore off at different rates in males of male-biased and female-biased regimes with increasing time from the removal of competitive cues. Furthermore, our study finds that males change their reproductive strategies depending upon the identity of rival males. Together, our results provide evidence of the evolution of male reproductive investment that depends on socio-sexual cues experienced early in life.

Extensive geographical variation in testes size and ejaculate traits in a terrestrial-breeding frog.

Ejaculate traits vary extensively among individuals and species, but little is known about their variation among populations of the same species. Here, we investigated patterns of intraspecific variation in male reproductive investment in the terrestrial-breeding frog Pseudophryne guentheri. Like most anurans, breeding activity in P. guentheri is cued by precipitation, and therefore the timing and duration of breeding seasons differ among geographically separated populations, potentially leading to differences in the level of sperm competition. We, therefore, anticipated local adaptation in sperm traits that reflect these phenological differences among populations. Our analysis of six natural populations across a rainfall gradient revealed significant divergence in testes and ejaculate traits that correspond with annual rainfall and rainfall seasonality; males from the northern and drier edge of the species range had significantly smaller testes containing fewer, smaller and less motile sperm compared with those from mesic central populations. These findings may reflect spatial variation in the strength of postcopulatory sexual selection, likely driven by local patterns of precipitation.

Hoopoe Upupa epops male feeding effort is related to female cosmetic egg colouration

Avian eggshell colouration might function as a post‐mating sexually selected signal of female quality, influencing male parental investment and, hence, reproductive success. This hypothesis has been tested for intrinsic eggshell pigments as biliverdin (blue‐green colouration) and/or protoporphyrin (brown coloured spots), but never for colourations applied post‐laying. Post‐laying staining colouration due to, for instance, uropygial secretion of the female could reflect its phenotypic properties and, thus, might be a cue for male investment in reproduction. In hoopoes, the uropygial gland of incubating females hosts symbiotic bacteria that are responsible for the brown colour of their uropygial secretion and of the eggshells, as they cover their bluish‐grey eggshells with gland secretion after laying. The secretion protects embryos from pathogenic trans‐shell infections and, thus, egg colouration may function as a cue or even as a post‐mating sexually selected signal of antimicrobial potential in hoopoes. In a wild hoopoe population breeding in nest boxes in Spain, we test this hypothesis by exploring whether egg colour predicts male parental investment. In accordance with the hypothesis, we found that the amount of food provided by males to incubating females was higher in nests with less saturated eggshell colours. This relationship was affected by female body condition. High quality females in terms of body condition and/or in secretion colour obtained better males in terms of provisioning effort during incubation. Given that eggshell saturation is negatively related to density of bacterial symbionts in uropygial secretions, one possibility is that males may regulate their parental investment in accordance to the expected characteristics of mutualistic bacteria hosted in uropygial glands and deposited on eggshells. We discuss alternative explanations for our results, concluding that the post‐mating sexual selection hypothesis is the most likely but experimental modification of egg colour is needed to test it further.

Anthropogenic noise reduces male reproductive investment in an acoustically signaling insect

Rapidly changing environments impose novel selection pressures on organisms, and sometimes adaptive phenotypic plasticity allows organisms to survive and reproduce in the face of environmental change. However, plastic responses can also be maladaptive. In this study, we investigate whether male reproductive investment responds plastically to varied experience with traffic noise. We exposed male crickets chronically to one of three noise treatments from the 2nd-3rd instar until their natural death: masking traffic noise (including noise that overlaps in frequency with the male crickets’ mating calls), non-masking traffic noise (an identical traffic noise track from which we digitally removed the frequencies that mask the crickets’ mating call), and silence. We dissected and weighed their testes and spermatophore molds. Controlling for body mass, we found that the spermatophore molds of crickets reared in masking and non-masking noise were 29% and 24% lighter, respectively, than those of crickets reared in silence. There were no differences in body mass-adjusted testes mass among treatments. If spermatophore mold mass is positively associated with male reproductive output, this reduction in size could have negative fitness consequences for animals exposed to traffic noise. We encourage future work to investigate impacts of noise on reproductive investment in other study systems that are likely sensitive to anthropogenic noise (e.g., birds, frogs, singing insects). Anthropogenic noise is a pervasive pollutant and chronic noise can negatively affect fitness. How does anthropogenic noise influence reproductive investment? Phenotypically plastic responses to noise may increase survival and reproduction in noisy environments. Traffic noise masks the sounds crickets make, potentially changing conspecifics’ perception of population density, mate availability, and the risk of sperm competition. We found that male crickets reared in silence developed significantly larger spermatophore molds (a reproductive structure that delivers the sperm containing packet to the female) than those reared in traffic noise. If the spermatophore mold influences male reproductive output, this reduction in size may have negative impacts on reproductive success of animals exposed to masking traffic noise.