Female Reproductive Investment Research Articles

Clutch Size, but Not Egg Volume, Increases with Rainfall in an Arid-dwelling Bird.

Understanding how animals maximize reproductive success in variable environments is important in determining how populations will respond to increasingly extreme weather events predicted in the face of changing climates. Although temperature is generally considered a key factor in reproductive decisions, rainfall is also an important predictor of prey availability in arid environments. Here, we test the impact of weather (i.e., rainfall and temperature) on female reproductive investment in an arid-dwelling bird (i.e., clutch size and egg volume) and tradeoffs between the two. We predicted that female chestnut-crowned babblers (Pomatostomus ruficeps), endemic to the arid region of Australia, would increase clutch size at the expense of egg volume in response to variation in rainfall and temperature. We found that over 14 breeding seasons, clutch size decreased with increasing temperature, but increased following more rain. Egg volume, on the other hand, became larger as temperatures increased and, although not related to the amount of rain, was related to the number of days since the last rainfall. Finally, egg size decreased as clutch size increased, indicating a tradeoff between the two reproductive parameters. Our results suggest that chestnut-crowned babblers breed reactively in response to variable environments. We expect that clutch size variation in response to rain may reflect the impact of rain on arthropod abundance, whereas the effect of temperature may represent an established decline in clutch size observed in other seasonal breeders. As the tradeoff between clutch size and egg volume was modest, and clutch sizes were modified to a greater extent than egg volumes in response to rainfall, we suggest selection is more likely to increase offspring number than quality, at least in favorable years. Our results support the idea that reproductive investment is variable in fluctuating environments, which has implications for species living in habitats experiencing more extreme and less predictable weather as the global climate changes.

Filling latitudinal gaps in Tachycineta swallows: reproductive strategies in a South American species

ABSTRACT Chilean swallows (Tachycineta leucopyga) are the southernmost swallows in the Tachycineta genus, breeding from central Chile to southern Chile and Argentina. Studies focused on a population breeding at 54°S in Tierra del Fuego, revealed differences in life-history traits compared to their Northern Hemisphere congeners, such as smaller clutch size, and greater male nest attendance during the incubation period. To assess the consistency of these patterns for the species, we studied breeding biology and parental care of Chilean swallows in Northwestern Argentine Patagonia (41°S). If austral population breeding traits reflect species traits, we predict smaller clutch size, higher female reproductive investment, and similar nest attendance by both sexes during incubation compared to Tachycineta species breeding at similar Northern Hemisphere latitudes. We also anticipate negative correlation between clutch size, egg size, and breeding success with laying date, as observed in Tachycineta species, including Chilean swallows. Surprisingly, clutch and egg sizes did not differ between northern and southern Patagonian populations. We did not find evidence of a negative relationship between clutch or egg size and laying date. Male nest attendance during incubation was variable and low, but their nestlings feeding rates equalled those of females. These findings suggest that Chilean swallows adopt diverse reproductive strategies across regions. This may help this species adapt to different environments and climates, ranging from the shorter breeding seasons and lower summer mean temperatures of Tierra del Fuego to the longer breeding seasons and higher seasonal and daily thermal amplitudes in continental north Andean Patagonia.

Effect of rearing density on female investment in reproduction and melanotic encapsulation response in the sand cricket (Gryllus firmus) (Orthoptera: Gryllidae)

Abstract The density-dependent prophylaxis hypothesis posits that because pathogens are expected to be transmitted among conspecifics in crowded conditions, individuals living in such conditions should minimize their chance of infection and maximize survival by elevating their baseline immunity. Further, if individuals developing in crowded conditions indeed allocate more resources to immunity then resource allocation to other life-history traits, such as reproduction, should decline. We tested these hypotheses by rearing sand crickets (Gryllus firmus) at either low or high density in the laboratory and quantified immune function (melanotic encapsulation response) and reproductive investment (ovary mass, egg size) at adulthood. The results did not support the density-dependent prophylaxis hypothesis, but we did find that rearing density significantly affected investment in two reproductive traits, with average ovary mass and egg size both being larger in low-density crickets. We discuss possible explanations for the lack of a trade-off between immunity and reproduction in our study.

Genetic basis and expression of ventral colour in polymorphic common lizards.

Colour is an important visual cue that can correlate with sex, behaviour, life history or ecological strategies, and has evolved divergently and convergently across animal lineages. Its genetic basis in non-model organisms is rarely known, but such information is vital for determining the drivers and mechanisms of colour evolution. Leveraging genetic admixture in a rare contact zone between oviparous and viviparous common lizards (Zootoca vivipara), we show that females (N = 558) of the two otherwise morphologically indistinguishable reproductive modes differ in their ventral colouration (from pale to vibrant yellow) and intensity of melanic patterning. We find no association between female colouration and reproductive investment, and no evidence for selection on colour. Using a combination of genetic mapping and transcriptomic evidence, we identified two candidate genes associated with ventral colour differentiation, DGAT2 and PMEL. These are genes known to be involved in carotenoid metabolism and melanin synthesis respectively. Ventral melanic spots were associated with two genomic regions, including a SNP close to protein tyrosine phosphatase (PTP) genes. Using genome re-sequencing data, our results show that fixed coding mutations in the candidate genes cannot account for differences in colouration. Taken together, our findings show that the evolution of ventral colouration and its associations across common lizard lineages is variable. A potential genetic mechanism explaining the flexibility of ventral colouration may be that colouration in common lizards, but also across squamates, is predominantly driven by regulatory genetic variation.

The impact of different pairing scheme on female reproductive investment: Research on Japanese Quail (Cortunix japonica)

Determining the sex of the embryo during incubation is crucial for the poultry industry. The primary problem to comprehend in this study is the manipulation of the sex ratio and also the egg production. The study will concentrate on how two distinct methods of pairing parents—one male with one female and another male with three females—affect egg production, the average egg mass, and the sex offspring ratio. As the animal model, we employ the layer strain of the Japanese Quail (Coturnix japonica) since they produce continuous eggs each day and easy to handle. The Japanese quail pairs were housed for seven days prior to the start of egg collection. These eggs were nurtured for up to three weeks after hatching until the sexing could be determined. When compared to a pair of three females, the egg production of a single pair was much higher when alternative pattern schemes were used. However, the mass of their typical eggs is remarkably similar. The male to female chick offspring sex ratio regularly showed to be 1:1 or equal. This finding could serve as the foundation for further research into the impact of partner pairing on another avian layer strain.

Whoever their partner, female blue tits breed the same

Abstract Do females modify their reproductive investment if they do not succeed in pairing with a male that matches their preference? In a two-year experiment, we asked female blue tits (Cyanistes caeruleus) to select among six males, and then successively paired them with their preferred and their most avoided male. We monitored female reproductive investment through nest building activity, timing of breeding, size and number of eggs, number of fertilized eggs, and brood sex ratio. We found that females preferred males with a chromatic coloration (blue UV chroma of the head crown) that matched their own, but also that they preferred males with a lower achromatic coloration (less bright color of the cheeks and head crown). Although females paired with their preferred males tended to build heavier nests during the breeding season, we found no evidence of an effect of the pairing treatment on timing of breeding, or any other aspects of female reproductive investment. We however found that laying dates, clutch sizes, egg sizes, and brood sex ratio were significantly repeatable within females between the two years, despite the opposite pairing treatments. These findings show that in female blue tits, the males with which they are paired do not substantially alter their reproductive decisions.

African striped mice have relatively smaller brains in the food deprived dry season than in the wet season

The ability to alter the mass of energetically consumptive organs in response to seasonal variation in nutritional access has been demonstrated in several species from temperate climates, but less so from other climate zones. We predicted that adult striped mice (Rhabdomys pumilio) from the Succulent Karoo semi-desert in South Africa have lower organ masses during the hot summer dry season with low food availability (n = 28) when compared to the food-rich wet season (n = 25) as a possible adaptation to reduced energy expenditure. Food availability in the wet season was more than twice than that of the dry season. Body mass was positively correlated with most organ masses considered, except for the spleen. Mandible length, as a non-plastic measure of body size, was positively correlated with the mass of heart and stomach. Relative to body mass and to mandible length, kidneys and the small intestine were heavier in the wet season than during the dry season in both sexes. Liver masses were greater in females (but smaller in males) during the wet season, possibly due to increased female reproductive investment during this season. Both sexes had relatively heavier brains (by 9.6% on average) during the wet season than during the dry season, which is the first indication of the Dehnel phenomenon in a rodent, in a subtropical climate, and in the southern hemisphere. Future studies will have to test whether this change in brain size is reversible. Having relatively smaller brains during the dry season could be a mechanism to reduce energy consumption. In conclusion, our study indicates that striped mice may save energy during the food restricted dry season by reducing energetically expensive organ masses, including brain mass.

Female investment in terminal reproduction or somatic maintenance depends on infection dose

Abstract Immune responses are energetically costly to produce and often trade off with investment in reproduction and offspring provisioning. We predicted that hosts can interpret the magnitude of the infection threat from cues like initial bacterial load to adjust reproductive investment into offspring quantity and quality. To test this prediction, we exposed female flour beetles (Tribolium castaneum) to naïve or sterile media controls or one of three increasing doses of heat‐killed Bacillus thuringiensis (Bt). To estimate offspring quantity, we measured the number of eggs and hatched larvae from each maternal treatment group. To estimate offspring quality, we measured egg protein content, development to pupation, pupal weight and offspring survival against Bt infection. Compared to naïve controls, low and intermediate bacterial doses resulted in lower female fecundity, suggesting a shift to a somatic maintenance strategy. Meanwhile, in the highest‐dose group, fecundity was negatively correlated with egg protein content. This may reflect a trade‐off between offspring quality and quantity that could mask terminal investment based on metrics of quantity alone. Our results underscore the need to account for the magnitude of environmental cues when quantifying plasticity and trade‐offs among life history traits, and provide new insight into the transgenerational effects of immune responses.

Sex bias in mortality risk changes over the lifespan of bottlenose dolphins.

Research on sex biases in longevity in mammals often assumes that male investment in competition results in a female survival advantage that is constant throughout life. We use 35 years of longitudinal data on 1003 wild bottlenose dolphins (Tursiops aduncus) to examine age-specific mortality, demonstrating a time-varying effect of sex on mortality hazard over the five-decade lifespan of a social mammal. Males are at higher risk of mortality than females during the juvenile period, but the gap between male and female mortality hazard closes in the mid-teens, coincident with the onset of female reproduction. Female mortality hazard is non-significantly higher than male mortality hazard in adulthood, resulting in a moderate male bias in the oldest age class. Bottlenose dolphins have an intensely male-competitive mating system, and juvenile male mortality has been linked to social competition. Contrary to predictions from sexual selection theory, however, male-male competition does not result in sustained male-biased mortality. As female dolphins experience high costs of sexual coercion in addition to long and energetically expensive periods of gestation and lactation, this suggests that substantial female investment in reproduction can elevate female mortality risk and impact sex biases in lifespan.

Increased male-induced harm in response to female-limited selection: interactive effects between intra- and interlocus sexual conflict?

Interlocus sexual conflict (IRSC) occurs because of shared interactions that have opposite effects on male and female fitness. Typically, it is assumed that loci involved in IRSC have sex-limited expression and are thus not directly affected by selective pressures acting on the other sex. However, if loci involved in IRSC have pleiotropic effects in the other sex, intersexual selection can shape the evolutionary dynamics of conflict escalation and resolution, as well as the evolution of reproductive traits linked to IRSC loci, and vice versa. Here we used an artificial selection approach in Japanese quail (Coturnix japonica) to test if female-limited selection on reproductive investment affects the amount of harm caused by males during mating. We found that males originating from lines selected for high female reproductive investment caused more oxidative damage in the female reproductive tract than males originating from lines selected for low female reproductive investment. This male-induced damage was specific to the oviduct and not found in other female tissues, suggesting that it was ejaculate-mediated. Our results suggest that intersexual selection shapes the evolution of IRSC and that male-induced harm may contribute to the maintenance of variation in female reproductive investment.

Stress tolerance is influenced by artificial light at night during development and life-history strategy.

Artificial light at night (ALAN) is increasingly prevalent worldwide, but life-history strategy may mitigate the costs of ALAN for animals. Yet, interactions among ALAN, life-history strategy and tolerance to climate-related stressors are unknown. We determined if developmental ALAN exposure (1) affects development, (2) affects adult phenotype, including heat and desiccation tolerance, and (3) affects and/or interacts with life-history strategy. We used the variable field cricket (Gryllus lineaticeps) because its geographic range is increasingly exposed to ALAN, heat, and drought conditions, and it exhibits different life-history strategies (flight-capability versus flight-incapability). ALAN affected adult phenotype, with positive effects on body mass (and size) and female reproductive investment, and a negative effect on heat tolerance. Life-history strategy also affected stress tolerance; flight-incapable females had greater heat tolerance and their desiccation tolerance was improved by ALAN exposure. Key features of environmental change (i.e. exposure to ALAN, heat and drought) may favor some life-history strategies over others.

Male plumage colouration predicts female reproductive investment and nestling survival in a colour dimorphic tropical songbird

In sexually colour dimorphic bird species, males can exhibit phenotypic variation, with males breeding in either dull female-like plumage or brightly coloured plumage. Two contradictory hypotheses predict that the male phenotype variation can influence the female investment in a given breeding attempt. Whereas females usually prefer males in bright coloured plumage, the “differential allocation hypothesis” predicts that females should invest more in their reproductive output when mating with them; while the “compensatory investment hypothesis” predicts that females should invest more when mating with non-preferred males. To test those predictions, we analysed reproductive data for two consecutive breeding seasons (2018–2019 and 2019–2020) of Lined Seedeaters Sporophila lineola. S. lineola is a socially monogamous songbird species in which males exhibit two breeding phenotypes, a black-and-white plumage being the most common, and a less common female-like brownish plumage. Our findings show that females mated with brownish males have a higher reproductive investment (i.e., egg volume) than those mated with black-and-white males. Despite the lower investment of females in egg volume, our results showed that black-and-white males have a higher nestling survival, producing more hatchings and fledglings per season than brownish males, which could suggest a higher fitness. Our findings indicate that investment allocation on the eggs and offspring survival rates can be attributed to the plumage colour of males.

Female choice of mates in the aphidophagous ladybird beetle, Hippodamia variegata (Coleoptera: Coccinellidae): the effect of male age, sexual status and familiarity

Mating involves the transfer of sperm to females. Female reproductive investment is based on gamete numbers as well as gamete size. Females are more selective than males and this selection is based on numerous factors, like a male’s age, sexual status and familiarity. Hippodamia variegata (Goeze) (Coleoptera: Coccinellidae) is an important natural enemy of many insect pests such as aphids, psyllids, whiteflies and mealybugs in many countries. We investigated female mate choice in Hippodamia variegate caging females with: (i) a young and a middle-aged male, (ii) a virgin and mated male and (iii) a novel and a familiar male. Time to and duration of copulation were recorded. Females preferred to mate with middle-aged and familiar males and did not differentiate between previously mated and virgin males. Females copulated quicker and for longer with young or familiar males.

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.

A single mating is sufficient to induce persistent reduction of immune defense in mated female Drosophila melanogaster

In many species, female reproductive investment comes at a cost to immunity and resistance to infection. Mated Drosophila melanogaster females are more susceptible to bacterial infection than unmated females. Transfer of the male seminal fluid protein Sex Peptide reduces female post-mating immune defense. Sex Peptide is known to cause both short- and long-term changes to female physiology and behavior. While previous studies showed that females were less resistant to bacterial infection as soon as 2.5 h and as long as 26.5 h after mating, it is unknown whether this is a binary switch from mated to unmated state or whether females can recover to unmated levels of immunity. It is additionally unknown whether repeated mating causes progressive reduction in defense capacity. We compared the immune defense of mated females when infected at 2, 4, 7, or 10 days after mating to that of unmated females and saw no recovery of immune capacity regardless of the length of time between mating and infection. Because D. melanogaster females can mate multiply, we additionally tested whether a second mating, and therefore a second transfer of seminal fluids, caused deeper reduction in immune performance. We found that females mated either once or twice before infection survived at equal proportions, both with significantly lower probability than unmated females. We conclude that a single mating event is sufficient to persistently suppress the female immune system. Interestingly, we observed that induced levels of expression of genes encoding antimicrobial peptides (AMPs) decreased with age in both experiments, partially obscuring the effects of mating. Collectively, the data indicate that being reproductively active versus reproductively inactive are alternative binary states with respect to female D. melanogaster immunity. The establishment of a suppressed immune status in reproductively active females can inform our understanding of the regulation of immune defense and the mechanisms of physiological trade-offs.

Multiple aspects of the maternal reproductive investment in a polytocous species: What do mothers really control?

One of the factors facilitating the expansion and proliferation of wild boar Sus scrofa is the plasticity of its reproductive biology. Nevertheless, the real influence of maternal and environmental factors on number and sex of the offspring is still controversial. While the litter size was shown to be related with the maternal condition, the strength of this relation remains to be understood, together with the possible role played by environmental conditions. Analogously, it is unclear whether wild boar females can adjust their offspring sex. We investigated multiple aspects of wild boar maternal investment by means of a 10-year dataset of female reproductive traits and a set of biologically meaningful environmental variables. The maternal condition slightly affected the litter size but not the offspring sex, and environment did not affect the litter size or the offspring sex. Moreover, mothers did not cope with the higher costs entailed by producing sons by placing them in the most advantageous intrauterine position, nor by allocating less resources on daughters. Our set of results showed that the female reproductive investment is quite rigid in comparison with other aspects of wild boar reproductive biology. Wild boar females seem to adopt a typical r-strategy, producing constantly large litters and allocating resources on both sexes regardless of internal and external conditions. Such strategy may be adaptive to cope with environmental unpredictability and an intense human harvest, contributing to explain the extreme success of wild boar within human-dominated landscapes.

Perspective: Re-defining "Pheromone" in a Mammalian Context to Encompass Seminal Fluid.

The classical view of “pheromone”—an air-borne chemical signal—is challenged by the camelids in which ovulation is triggered by ß-nerve growth factor carried in seminal plasma, effectively extending the pheromone concept to a new medium. We propose further extension of “pheromone” to include a separate class of seminal fluid molecules that acts on the female reproductive tract to enhance the prospect of pregnancy. These molecules include transforming growth factor-ß, 19-OH prostaglandins, various ligands of Toll-like receptor-4 (TLR4), and cyclic ADP ribose hydrolase (CD38). They modulate the immune response to “foreign” male-derived histocompatibility antigens on both sperm and the conceptus, determine pre-implantation embryo development, and then promote implantation by increasing uterine receptivity to the embryo. The relative abundance of these immunological molecules in seminal plasma determines the strength and quality of the immune tolerance that is generated in the female. This phenomenon has profound implications in reproductive biology because it provides a pathway, independent of the fertilizing sperm, by which paternal factors can influence the likelihood of reproductive success, as well as the phenotype and health status of offspring. Moreover, the female actively participates in this exchange—information in seminal fluid is subject to “cryptic female choice,” a process by which females interrogate the reproductive fitness of prospective mates and invest reproductive resources accordingly. These processes participate in driving the evolution of male accessory glands, ensuring optimal female reproductive investment and maximal progeny fitness. An expanded pheromone concept will avoid a constraint in our understanding of mammalian reproductive biology.

Ecological and phylogenetic constraints determine the stage of anthetic ovule development in orchids.

Unlike most flowering plants, orchid flowers have under-developed ovules that complete development only after pollination. Classical studies reported variation in the stage in which ovule development is arrested, but the extent of this variation and its evolutionary and ecological significance are unclear. Here, we used light microscopy to observe ovule development at anthesis for 39 species not previously studied and surveyed the literature gaining information on 94 orchid species. Tropical and temperate members of all five orchid subfamilies as well as species with contrasting pollination strategies (rewarding versus deceptive) and life forms (epiphytic versus terrestrial) were represented. We analyzed the data using statistical comparisons and a phylogenetic generalized least square (PGLS) analysis. Apostasioideae, the sister to the rest of the orchids, have mature ovules similar to other Asparagales, while under-differentiated ovules are present in the other subfamilies. Ovule developmental stages showed high variation even among closely related groups. Ovules were more developed in terrestrial than in epiphytic, in temperate than in tropical, and in rewarding than in deceptive pollination orchid species. This latter comparison was also significant in the PGLS analysis. These results suggest that ovule developmental stage in orchids can be shaped by ecological factors, such as seasonality and pollination strategy, and can be selected for optimizing female reproductive investment.

Exposure to a mixture of benzo[a]pyrene and triclosan induces multi-and transgenerational metabolic disorders associated with decreased female investment in reproduction in Silurana (Xenopus) tropicalis

Animals must partition limited resources between their own growth and subsequent reproduction. Endocrine disruptors (ED) may cause maternal metabolic disorders that decrease successful reproduction and might be responsible for multi- and transgenerational effects in amphibians. We found that the frog Silurana (Xenopus) tropicalis, exposed to environmentally relevant concentrations of benzo[a]pyrene and triclosan throughout its life cycle, produced F1 females with delayed sexual maturity and decreased size and weight. These F1 females displayed a marked metabolic syndrome associated with decreased fasting plasma cholesterol and triglyceride concentrations and decreased gonadal development. F1 females from F0 exposed animals also had decreased reproductive investment highlighted by a decrease of oocyte lipid reserves associated with significant F2-tadpole mortality. F2 females from F0 exposed animals also displayed a marked metabolic syndrome but were able to correctly direct liver lipid metabolism to the constitution of fat bodies and oocyte yolk stores. In addition, the F2 females produced progeny that had normal mortality levels at 5 days post hatching compared to the controls suggesting a good reproductive investment. Our data confirmed that these ED, at concentrations often found in natural ponds, can induce multi- and transgenerational metabolic disorders in the progeny of amphibians that are not directly exposed. We present a hypothesis to explain the transmission of the metabolic syndrome across generations through modification of egg reserves. However, when high mortality occurred at the tadpole stage, surviving females were able to cope with metabolic costs and produce viable progeny through sufficient investment in the contents of oocyte reserves.

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.