Female Reproductive Success Research Articles

Little brown Myotis roosts are spatially associated with foraging resources on Prince Edward Island

AbstractAnimal fitness is closely linked to accessing and capitalizing on local resources such as prey and shelter. Resources vary in quality, thus individuals may demonstrate selectivity for particular resource types. We examined resource selection in roost selection patterns of temperate bats on Prince Edward Island. To complement existing work examining roost structural characteristics, we evaluated whether roost selection by little brown myotis (Myotis lucifugus) could be explained by landscape characteristics. Given a sample of roosts identified through radio telemetry, community reports and a randomly selected sample of comparison structures, we determined that a combination of proximity to forest and open wetland best explained roost selection. Roost selection appears to reflect the optimization of time and energy budgets, and the proportion of maternity roosts within the sample suggests that these constraints may be more acute in reproductive females. Given the importance of roosts for reproductive success in females, future work should seek to quantify the role of physical characteristics on roost structure selection and the preservation of suitable roosting structures.

Identification of familial networks reveals sex-specific density dependence in the dispersal and reproductive success of an endangered ungulate

Density is an important demographic parameter that is commonly overlooked in studies of wild populations. Here, we examined the effects of variable spatially explicit density on a range of demographic parameters in a wild population of a cryptic ungulate, boreal woodland caribou (Rangifer tarandus caribou). Using non-invasive genetic sampling, we applied spatial capture–recapture methods with landscape covariates to estimate the density of boreal woodland caribou across a 108,806 km2 study area. We then created a familial network from the reconstructed parent–offspring relationships to determine whether spatial density influenced sex-specific individual reproductive success, female pregnancy status, and dispersal distance. We found that animal density varied greatly in response to land cover types and disturbance; animal density was most influenced by landscape composition and distance to roads varying from 0 in areas with >20% deciduous cover to 270 caribou per 1,000 km2 in areas presenting contiguous older coniferous cover. We found that both male and female reproductive success varied with density, with males showing a higher probability of having offspring in higher-density areas, and the opposite for females. No differences were found in female pregnancy rates occurring in high- and low-density areas. Dispersal distances varied with density, with offspring moving shorter distances when parents were found in higher-density areas. Familial networks showed lower-closeness centrality and lower-degree centrality for females in higher-density areas, indicating that females found in higher-density areas tend to be less broadly associated with animals across the range. Although high-density areas do reflect good-quality caribou habitat, the observed decreased closeness and degree centrality measures, dispersal rates, and lower female recruitment rates suggest that remnant habitat patches across the landscape may create population sinks.

Multilevel selection on social network traits differs between sexes in experimental populations of forked fungus beetles

Both individual and group behavior can influence individual fitness, but multilevel selection is rarely quantified on social behaviors. Social networks provide a unique opportunity to study multilevel selection on social behaviors, as they describe complex social traits and patterns of interaction at both the individual and group levels. In this study, we used contextual analysis to measure the consequences of both individual network position and group network structure on individual fitness in experimental populations of forked fungus beetles (Bolitotherus cornutus) with two different resource distributions. We found that males with high individual connectivity (strength) and centrality (betweenness) had higher mating success. However, group network structure did not influence their mating success. Conversely, we found that individual network position had no effect on female reproductive success but that females in populations with many social interactions experienced lower reproductive success. The strength of individual-level selection in males and group-level selection in females intensified when resources were clumped together, showing that habitat structure influences multilevel selection. Individual and emergent group social behavior both influence variation in components of individual fitness, but impact the male mating success and female reproductive success differently, setting up intersexual conflicts over patterns of social interactions at multiple levels.

Sex-dependent effects of parental age on offspring fitness in a cooperatively breeding bird.

Parental age can have considerable effects on offspring phenotypes and health. However, intergenerational effects may also have longer term effects on offspring fitness. Few studies have investigated parental age effects on offspring fitness in natural populations while also testing for sex- and environment-specific effects. Further, longitudinal parental age effects may be masked by population-level processes such as the selective disappearance of poor-quality individuals. Here, we used multigenerational data collected on individually marked Seychelles warblers (Acrocephalus sechellensis) to investigate the impact of maternal and paternal age on offspring life span and lifetime reproductive success. We found negative effects of maternal age on female offspring life span and lifetime reproductive success, which were driven by within-mother effects. There was no difference in annual reproductive output of females born to older versus younger mothers, suggesting that the differences in offspring lifetime reproductive success were driven by effects on offspring life span. In contrast, there was no association between paternal age and female offspring life span or either maternal or paternal age and male offspring life span. Lifetime reproductive success, but not annual reproductive success, of male offspring increased with maternal age, but this was driven by between-mother effects. No paternal age effects were found on female offspring lifetime reproductive success but there was a positive between-father effect on male offspring lifetime reproductive success. We did not find strong evidence for environment-dependent parental age effects. Our study provides evidence for parental age effects on the lifetime fitness of offspring and shows that such effects can be sex dependent. These results add to the growing literature indicating the importance of intergenerational effects on long-term offspring performance and highlight that these effects can be an important driver of variation in longevity and fitness in the wild.

On the function of flower number: disentangling fertility from pollinator-mediated selection.

In animal-pollinated angiosperms, the 'male-function' hypothesis claims that male reproductive success (RS) should benefit from large floral displays, through pollinator attraction, while female RS is expected to be mainly limited by resource availability. As appealing as this theory might be, studies comparing selection strength on flower number in both sexes rarely document the expected asymmetry. This discrepancy could arise because flower number impacts both pollinator attraction and overall gamete number. In this study, we artificially manipulate floral displays to disentangle the fertility versus pollinator attraction components of selection, both in terms of mating and RS. In females, flower number was under strong fertility selection, as predicted in the absence of pollen limitation. By contrast, in males, flower number was mainly under sexual selection, which in turn increased male RS. However, these selection patterns were not different in males with artificially increased floral displays. This suggests that sexual selection acting on flower number in males does not occur because flower number increases pollinator attraction, but rather because more pollen is available to disperse on more mates. Our study illustrates the power of disentangling various components of selection with potentially sex-specific effects for understanding the evolution of sexual dimorphism.

Sexual selection moderates heat stress response in males and females.

A widespread effect of climate change is the displacement of organisms from their thermal optima. The associated thermal stress imposed by climate change has been argued to have a particularly strong impact on male reproduction but evidence for this postulated sex-specific stress response is equivocal.One important factor that may explain intra- and interspecific variation in stress responses is sexual selection, which is predicted to magnify negative effects of stress. Nevertheless, empirical studies exploring the interplay of sexual selection and heat stress are still scarce.We tested experimentally for an interaction between sexual selection and thermal stress in the red flour beetle Tribolium castaneum by contrasting heat responses in male and female reproductive success between enforced monogamy and polygamy.We found that polygamy magnifies detrimental effects of heat stress in males but relaxes the observed negative effects in females. Our results suggest that sexual selection can reverse sex differences in thermal sensitivity, and may therefore alter sex-specific selection on alleles associated with heat tolerance.Assuming that sexual selection and natural selection are aligned to favour the same genetic variants under environmental stress, our findings support the idea that sexual selection on males may promote the adaptation to current global warming. Read the free Plain Language Summary for this article on the Journal blog.

Cascading effects of social dynamics on the reproduction, survival, and population growth of mountain gorillas

AbstractWhilst the conservation impacts of density‐dependent population effects have been well studied, the impact that socially‐driven changes (e.g. group fissions that increase group density) can have on population growth in social species have only recently come to light. An increase in group density and intergroup encounters in a subpopulation of mountain gorillas Gorilla beringei beringei was shown to have driven a more than fourfold increase in infanticide, slowing population growth. In this study, we delve deeper into the consequences of these socially‐driven changes in group density, examining how patterns of reproduction and survival have changed in this subpopulation across more than 50 years. We show that adult female survival increased with strengthening conservation efforts early in the study, then remained stable, while age at first birth remained stable across the entire study. Interbirth intervals and female reproductive success did not vary significantly across time overall. However, socially‐driven increases in group density since the mid‐2000s appear to have had a cascade of effects. In addition to the increase in infant and adult male mortality from violence during intergroup encounters, higher encounter rates, and mortality were likely responsible for an increase in female transfers, which delayed reproduction. Females faced a 7.5‐month delay when transferring once and a 1.5‐year delay when transferring twice or more between births. We show these changes correspond with a 26.63% reduction in female reproductive success in 2007 to 2018, compared to 1994 to 2006, with females taking more than 2 years longer to produce an offspring that survived infancy. These findings demonstrate that social dynamics can have consequences for population growth beyond the immediate mortality effects of violent encounters. This further highlights the critical importance of social dynamics in the conservation of social species, particularly when populations are restricted to small or fragmented regions of habitat.

Population dynamics of western gorillas at Mbeli Bai.

Long-term studies of population dynamics can provide insights into life history theory, population ecology, socioecology, conservation biology and wildlife management. Here we examine 25 years of population dynamics of western gorillas at Mbeli Bai, a swampy forest clearing in Nouabalé-Ndoki National Park, the Republic of Congo. The Mbeli population more than doubled from 101 to 226 gorillas during the study. After adjusting for a net influx of gorillas into the study population, the increase represents an inherent growth rate of 0.7% per year, with 95% confidence limits between -0.7% and 2.6%. The influx of gorillas mainly involved immigration of individuals into existing study groups (social dispersal), but it also included the appearance of a few previously unknown groups (locational dispersal). The average group size did not change significantly during the study, which is consistent with the possibility that western gorillas face socioecological constraints on group size, even when the population is increasing. We found no significant evidence of density dependence on female reproductive success or male mating competition. The distribution of gorillas among age/sex categories also did not change significantly, which suggests that the population had a stable age structure. Our results provide evidence of population stability or growth for some western gorillas (albeit within a small area). The results highlight the value of law enforcement, long-term monitoring, and protected areas; but they do not diminish the importance of improving conservation for this critically endangered species.

Infection with a Recently Discovered Gammaherpesvirus Variant in European Badgers, Meles meles, is Associated with Higher Relative Viral Loads in Blood.

Herpesviruses are ubiquitous pathogens infecting most animals. Although host immunity continually coevolves to combat virulence, viral variants with enhanced transmissibility or virulence occasionally emerge, resulting in disease burdens in host populations. Mustelid gammaherpesvirus 1 (MusGHV-1) is the only herpesvirus species identified thus far in European badgers, Meles meles. No MusGHV-1 associated pathomorbidity has been reported, but reactivation of MusGHV-1 in genital tracts is linked to impaired female reproductive success. An analysis of a short sequence from the highly conserved DNA polymerase (DNApol) gene previously identified two variants in a single host population. Here we compared genetic variance in blood samples from 66 known individuals of this same free-ranging badger population using a partial sequence comprising 2874 nucleotides of the DNApol gene, among which we identified 15 nucleotide differences resulting in 5 amino acid differences. Prevalence was 86% (59/66) for the common and 17% (11/66) for the novel variant, with 6% (4/66) of badgers presenting with coinfection. MusGHV-1 variants were distributed unevenly across the population, with individuals infected with the novel genotype clustered in 3 of 25 contiguous social groups. Individuals infected with the novel variant had significantly higher MusGHV-1 viral loads in their blood (p = 0.002) after adjusting for age (juveniles > adults, p < 0.001) and season (summer > spring and autumn, p = 0.005; mixed-effect linear regression), likely indicating higher virulence of the novel variant. Further genome-wide analyses of MusGHV-1 host resistance genes and host phenotypic variations are required to clarify the drivers and sequelae of this new MusGHV-1 variant.

Experimental evidence that group size generates divergent benefits of cooperative breeding for male and female ostriches.

Cooperative breeding allows the costs of parental care to be shared, but as groups become larger, such benefits often decline as competition increases and group cohesion breaks down. The counteracting forces of cooperation and competition are predicted to select for an optimal group size, but variation in groups is ubiquitous across cooperative breeding animals. Here, we experimentally test if group sizes vary because of sex differences in the costs and benefits of cooperative breeding in captive ostriches, Struthio camelus, and compare this to the distribution of group sizes in the wild. We established 96 groups with different numbers of males (1 or 3) and females (1, 3, 4, or 6) and manipulated opportunities for cooperation over incubation. There was a clear optimal group size for males (one male with four or more females) that was explained by high costs of competition and negligible benefits of cooperation. Conversely, female reproductive success was maximised across a range of group sizes due to the benefits of cooperation with male and female group members. Reproductive success in intermediate sized groups was low for both males and females due to sexual conflict over the timing of mating and incubation. Our experiments show that sex differences in cooperation and competition can explain group size variation in cooperative breeders.

Disruptive selection via pollinators and seed predators on the height of flowers on a wind-dispersed alpine herb.

Floral stalk height is known to affect seed dispersal of wind-dispersed grassland species, but it may also affect the attractiveness of flowers and fruits of animal-pollinated and animal-dispersed plants. Stalk height may thus be responsive to selection via interactions with both mutualist pollinators and seed dispersers, but also antagonist florivores and seed predators. In this study, we aimed to determine the effect of pollinators and seed predators on selection on floral stalk height in the insect-pollinated and wind-dispersed, alpine, andromonoecious herb Pulsatilla alpina, whose flowers also vary in their sex allocation and thus in the resources available to both mutualists and antagonists. We measured the resource status of individuals in terms of their size and the height of the vegetation surrounding plants of P. alpina at 11 sites. In one population, we recorded floral stalk height over an entire growing season and investigated its association with floral morphology and floral sex allocation (pistil and stamen number) and used leaf-removal manipulations to assess the effect of herbivory on floral stalk height. Finally, in four populations, we quantified phenotypic selection on floral stalk height in four female components of reproductive success before seed dispersal. Stalk height was positively associated with female allocation of the respective flower, the resource status of the individual, and the height of the surrounding vegetation, and negatively affected by leaf removal. Our results point to disruptive selection on stalk height in terms of both selection differentials and selection gradients for fertilization, seed predation, and seed maturation rates and to positive selection on stalk height in terms of a selection differential for mature seed number. Stalk height of P. alpina is a costly trait that affects female reproductive success via interactions with both mutualists and antagonists. We discuss the interplay between the resource status and selection imposed on female reproductive success and its likely role in the evolution of sex-allocation strategies, especially andromonoecy.

The effect of dominance rank on female reproductive success in social mammals

The effect of dominance rank on female reproductive success in social mammals

The influence of self-pollen deposition on female reproductive success in a self-incompatible plant, Akebia quinata.

Geitonogamy is inevitable in hermaphrodite and monecious. Even for self-incompatible species, the negative effects of self-pollen are unavoidable when geitonogamous or self-mating occurs. However, the influence of self-pollen on consecutive development of flowers (e.g., fruiting and seeding) was seldom evaluated. Here, the self-incompatible monecious species, Akebia quinata, was used to estimate the influence of self-pollen deposition. We evaluated the extent of pollen limitation and geitonogamous mating under natural conditions by count of stigmatic pollen load and pollen tracking experiment. Hand pollination with different amount and combinations of self vs. cross pollen grains was applied to detect the response of fruit and seed set. The results showed that geitonogamy and pollen limitation occurred under natural conditions in A. quinata. Carpel numbers, ratio of self- and cross-pollen, and the interactive effect of ratio of self- and cross-pollen and total mixed pollen numbers, and not total pollen grain number, determined the effect of self-pollen on female reproductive success. The effect of self-pollen depended on its intensity. In general, the transfer of self-pollen significantly affected young fruit set. However, a little self-pollen together with cross-pollen did not reduce young fruit production. Although self-incompatible plants have evolved physiological mechanisms that reduce self-fertilization, our results provide new insights into the effects of self-pollen and the adaptive significance of self-incompatible monecious species.

Structural anther mimics improve reproductive success through dishonest signaling that enhances both attraction and the morphological fit of pollinators with flowers.

Numerous studies have identified traits associated with anther mimicry; however, the processes underlying floral deception remain poorly documented for these structures. We studied the importance of pollinator attraction and mechanical fit of anther mimics in Tritonia laxifolia (Iridaceae) and their relative contributions to reproductive success. To determine anther mimics role in attraction, we offered bees’ binary choices to flowers painted with UV‐absorbent and UV‐reflecting paints. We also conducted preference experiments between flowers with excised anther mimics and unmanipulated controls, from which mechanical fit was assessed by allowing single visits. Anther mimics’ effects on female reproductive success were determined using similar treatments, but on rooted plants. Bees preferred UV‐absorbent over UV‐reflecting anther mimics. Bees did not discriminate between flowers with and without three‐dimensional anther mimics. Single visits resulted in more pollen deposition on unmanipulated controls over flowers with their anther mimics excised, which was directly linked to pollen‐collecting behavior. Controls with unmanipulated anther mimics had higher seed set than those with their anther mimics excised. This study provides insights into pollinator‐mediated selection on deceptive floral signals and shows that three‐dimensional anther mimics increases reproductive success through both attraction and pollen‐collecting behaviors.

Multigenerational Social Housing and Group-Rearing Enhance Female Reproductive Success in Captive Rhesus Macaques (Macaca mulatta).

Simple SummaryIt is currently common practice to house non-human primates at biomedical research facilities, e.g., rhesus macaques, in social groups. To enhance female reproductive success, peer groups are formed. In these breeding groups, infants are taken from their mother at an age of ten months and housed with animals of approximately the same age. Yet for welfare, leaving offspring with their mother and allowing multigenerational groups including families is preferred. This argues that a trade-off between female reproductive success and welfare exists. In this retrospective study we investigated the differences in female rhesus macaque reproductive success between peer groups and multigenerational groups. Our results show that females in multigenerational groups have more births per year and have higher offspring survival compared with those in peer groups. Thus, housing rhesus macaques in multigenerational groups provides a win−win situation, rather than a trade-off, in which female reproductive success and animal welfare can simultaneously be optimized.To optimize costs and reproductive success, rhesus macaques in biomedical primate research facilities are often peer-reared. Older, dependent infants are typically removed from their natal group to enhance female reproduction. The minimal husbandry age-norm of infant removal is ten months. These practices deviate from species-specific behavior and may reduce welfare, suggesting a trade-off between female reproduction and welfare. However, the effect of breeding group type and rearing history on female reproductive success (i.e., birth rate; inter-birth interval (IBI); offspring survival) is unclear. This retrospective study investigated whether group type (i.e., peer groups versus multigenerational groups) and rearing history (i.e., peer- or hand-reared; group-reared with peer- or hand-reared mother; group-reared) affected female reproductive success in captive rhesus macaques. Data on female reproduction between 1996 and 2019 were collected at the Biomedical Primate Research Centre, Rijswijk. Birth rates were higher in multigenerational breeding groups than in peer groups. Moreover, group-reared females had higher offspring survival than peer- or hand-reared females. IBI was not affected by breeding group type or female rearing history. However, females in both peer and multigenerational breeding groups typically conceived earlier after giving birth than the husbandry infant removal age-norm of ten months. Thus, infant removal at an age of ten months does not enhance a female’s reproduction. Altogether, female reproduction and non-human primate welfare can simultaneously be optimized through multigenerational breeding groups and group-rearing.

Pollen transfer and patterns of reproductive success in pure and mixed populations of nectariferous Platanthera bifolia and P. chlorantha (Orchidaceae).

Plant species evolution is driven by many factors that have different roles in space and time. Using different field and laboratory methods, we studied reproductive patterns and their determinants in pure and mixed P. bifolia and P. chlorantha populations in different habitats. We also considered the probability of hybridisation between these two species and the role of intra-population processes in maintaining species integrity. Generally, we found a high level of reproductive success in both Platantherans. In both species, male (MRS) and female (FRS) reproductive success depended on floral display, and male reproductive success additionally on population structure. The flower traits were only weakly related to reproductive success. Moths’ assemblages varied spatially and temporally, and their diversity and numbers were correlated with MRS in the year, when their abundance was markedly lower. Analysis of patterns of pollen transfer showed that pollen was transported up to 25 m (average 8.2 ± 4.83 m) and showed gene exchange between these two Platanthera species. The germination level of both species was significantly lower than seed viability, although P. bifolia seed germinated with higher frequency than P. chlorantha seeds. We noted differences in viability and germination of seeds developed as an effect of experimental interspecies crossings and those developed from natural pollination. The presence of intermediate ecotypes together with observations of spontaneous interspecies crosses in the field and viability of seeds produced in interspecies crossing suggest that both pre- and postzygotic reproductive barriers are not complete and do not prevent hybrid production.

From individual responses to population effects: Integrating a decade of multidisciplinary research on blue whales and sonar

AbstractAs ecosystems transform under climate change and expanding human activities, multidisciplinary integration of empirical research, conceptual frameworks and modelling methods is required to predict, monitor and manage the cascading effects on wildlife populations. For example, exposure to anthropogenic noise can lead to changes in the behaviour and physiology of individual marine mammals, but management is complicated by uncertainties on the long‐term effects at a population level. We build on a decade of diverse efforts to demonstrate the strengths of integrating research on multiple stressors for assessing population‐level effects. Using the case study of blue whales exposed to military sonar in the eastern north Pacific, we model how behavioural responses and environmental effects induced by climate change affect female survival and reproductive success. Environmental changes were predicted to severely affect vital rates, while the current regime of sonar activities was not. Simulated disturbance had a stronger effect on reproductive success than adult survival, as predicted by life‐history theory. We show that information on prey resources is critical for robust predictions, as are data on baseline behavioural patterns, energy budgets, body condition and contextual responses to noise. These results will support effective management of the interactions between sonar operations and blue whales in the study area, while providing pragmatic guidance for future data collection to reduce key uncertainties. Our study provides important lessons for the successful integration of multidisciplinary research to inform the assessment of the effects of noise and other anthropogenic stressors on marine predator populations in the context of a changing environment.

Increasing chronic anthropogenic disturbances and aridity differentially impact pollen traits and female reproductive success of Tacinga palmadora (Cactaceae) in a Caatinga dry forest

Increasing chronic anthropogenic disturbances and aridity differentially impact pollen traits and female reproductive success of Tacinga palmadora (Cactaceae) in a Caatinga dry forest

Local Insect Availability Partly Explains Geographical Differences in Floral Visitor Assemblages of Arum maculatum L. (Araceae).

Geographical variation in abundance and composition of pollinator assemblages may result in variable selection pressures among plant populations and drive plant diversification. However, there is limited knowledge on whether differences in local visitor and pollinator assemblages are the result of site-specific strategies of plants to interact with their pollinators and/or merely reflect the pollinator availability at a given locality. To address this question, we compared locally available insect communities obtained by light-trapping with assemblages of floral visitors in populations of Arum maculatum (Araceae) from north vs. south of the Alps. We further investigated whether and how the abundance of different visitors affects plants’ female reproductive success and examined the pollen loads of abundant visitors. Local insect availability explained inter-regional differences in total visitor abundance, but only partly the composition of visitor assemblages. Northern populations predominantly attracted females of Psychoda phalaenoides (Psychodidae, Diptera), reflecting the high availability of this moth fly in this region. More generalized visitor assemblages, including other psychodid and non-psychodid groups, were observed in the south, where the availability of P. phalaenoides/Psychodidae was limited. Fruit set was higher in the north than in the south but correlated positively in both regions with the abundance of total visitors and psychodids; in the north, however, this relationship disappeared when visitor abundances were too high. High pollen loads were recorded on both psychodids and other Diptera. We demonstrate for the first time that the quantitative assessment of floral visitor assemblages in relation to locally available insect communities is helpful to understand patterns of geographical variation in plant–pollinator interactions. This combined approach revealed that geographical differences in floral visitors of A. maculatum are only partly shaped by the local insect availability. Potential other factors that may contribute to the geographical pattern of visitor assemblages include the region-specific attractiveness of this plant species to flower visitors and the population-specific behavior of pollinators.

Highlighted articles for March 2022.

Highlighted articles for March 2022.