Reproductive Investment Research Articles

Recent declines in American lobster fecundity in southern New England: drivers and implications

Abstract Lobsters in southern New England (SNE) have experienced decades of environmental stressors along with a suite of emerging diseases. We hypothesized that the sublethal effects of physiological stress resulting from increased temperatures have contributed to a decline in reproductive investment in SNE lobsters. Using the presence of epizootic shell disease (ESD) as a proxy for stress, we examined lobster potential fecundity through the number of recently extruded, early-stage eggs and their nutritional quality; realized fecundity based on counts of late-stage eggs nearing hatch; and compared realized fecundity to historical data (1980s) from the region. Generalized linear modeling revealed that female size was a significant predictor of both potential and realized fecundity as expected, but that ESD status did not result in differences in fecundity. Dry weight was the only difference in nutritional content egg–1 between non-diseased and diseased females. There was also no relationship detected between potential fecundity and any nutritional metric from non-diseased females. However, both dry weight and protein were negatively correlated with potential fecundity in diseased females. Most importantly, realized fecundity of recent-day females was significantly reduced compared to the fecundity of historical females, characterized as a 23% decrease predicted by our model. Stressful environmental conditions, particularly temperature, may have contributed to decreased fecundity over a 30-year period in SNE. Our data demonstrate that expectations around the potential for the SNE stock to rebuild need to be adjusted to this new regime of decreased reproductive output and can no longer rely on past estimates of egg production and recruitment.

Effects of population density on adult morphology and life-history traits of female Mediterranean flour moth, Ephestia kuehniella (Lepidoptera: Pyralidae)

Intraspecific competition and food shortage due to high population density during early life can have a profound effect on adult fitness. Organisms often mitigate negative effects of high population density by adjusting resource allocation to adult morphological and life-history traits. In Lepidoptera with short-lived adults that do not feed, it is predicted that females developed from dense larval aggregations invest more in reproduction and traits linked to offspring survival. Here, we investigated the effects of larval population density on adult morphology and life-history traits in the female Mediterranean flour moth, Ephestia kuehniella by raising larvae at a range of population densities. Adults from high population density (16 larvae per g of food) had smaller head, thorax, and forewing compared to other densities. The allometric slope of forewing length with body mass did not differ among population densities, indicating no changes in adult wing morphology at high population density. However, we found that females emerged from larvae at high population density had bigger abdomens relative to body mass, indicating resource investment in reproduction, probably to mitigate the negative effects of crowding on egg production. Ovipositor length did not differ among population densities, indicating conservation of resources to structures with egg-laying function that affect offspring survival. Taken together, these results suggest that female E. kuehniella responding to high larval population density invest relatively more in reproduction, a life-history strategy that could alleviate negative effects of population density on fitness. This study also highlights the importance of a species' reproductive strategy in its adaptive response to environmental conditions, which is relevant to many capital breeders dependent on larval resources for reproduction.

Pesticides in a warmer world: Effects of glyphosate and warming across insect life stages

Glyphosate (GLY) is a broad-spectrum herbicide that is the most commonly applied pesticide in terrestrial ecosystems in the U.S. and, potentially, worldwide. However, the combined effects of warming associated with climate change and exposure to GLY and GLY-based formulations (GBFs) on terrestrial animals are poorly understood. Animals progress through several life stages (e.g., embryonic, larval, and juvenile stages) that may exhibit different sensitivities to stressors. Therefore, we factorially manipulated temperature and GLY/GBF exposure in the variable field cricket (Gryllus lineaticeps) during two life stages—nymphal development and adulthood—and examined key animal traits, such as developmental rate, body size, food consumption, reproductive investment, and lifespan. A thermal environment simulating future climate warming obligated several costs to fitness-related traits. For example, warming experienced during nymphal development reduced survival, adult body mass and size, and investment into flight capacity and reproduction. Warming experienced by adults reduced lifespan and growth rate. Alternatively, the effects of GBF exposure were more subtle, often context-dependent (e.g., effects were only detected in one sex or temperature regime), and were stronger during adult exposure relative to exposure during development. There was evidence of additive costs of warming and GBF exposure to rates of feeding and growth in adults. Yet, the negative effect of GBF exposure to adult lifespan did not occur in warming conditions, suggesting that ongoing climate change may obscure some of the costs of GBFs to non-target organisms. The effects of GLY alone (i.e., in the absence of proprietary surfactants found in commercial formulations) were non-existent. Animals will be increasingly exposed to warming and GBFs, and our results indicate that GBF exposure and warming can entail additive costs for an animal taxon (insects) that plays critical roles in terrestrial ecosystems.

Carry‐over effects on reproduction in food‐supplemented wintering great tits

Bird winter‐feeding has become a popular backyard activity around the world, particularly in northern regions of Europe and America with cold winters. However, the short‐ and long‐term ecological consequences of such artificial feeding remain inconclusive. In seasonal environments, timing of breeding is a crucial aspect that can strongly influence reproductive output and ultimately fitness. Individual condition at the start of the breeding season is especially important in determining breeding success, by influencing the onset of and investment in breeding. However, empirical evidence on the effects of winter feeding on avian breeding performance remain equivocal.We studied onset of reproduction (laying date) and breeding investment (clutch size) over seven consecutive seasons in a population of wild great tits Parus major in southern Sweden. During the first three years of study, no experimental manipulation was undertaken, while over the last four years the study area was exposed to either supplemented or unmanipulated winter feeding conditions. Breeding was positively affected by supplementary feeding during winter, as birds breeding in the supplemented area increased their clutch size compared to birds from the control area, although laying date remained unaffected by winter feeding. Since differences in clutch size were absent during the three years prior to the experimental manipulation, the results suggest that winter supplementary feeding, and not inherent differences between the two areas, was the reason for the observed effect. Both breeding parameters varied over the years of study, although the effects of the experimental manipulation on clutch size remained consistent, which suggests a carry‐over effect of winter feeding on subsequent breeding performance.

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.

The Immunological and Oxidative Costs of Reproduction and Associations between Maternal and Egg Yolk Physiology in a Reptile

Energetic constraints caused by reproductive investment may incur immunological and oxidative costs to a female and potentially to her developing offspring. Oviparous reptiles are capable of altering offspring phenotype through differential allocation of physiological factors during vitellogenesis (yolk formation), depending upon the external environment and the physiological state of the female. Despite its importance in protecting developing offspring against infection, maternal transfer of immune factors has rarely been studied in reptiles. Furthermore, the extent to which offspring may be impacted by the inherent oxidative costs of vitellogenesis is not well understood. Using the Side-blotched Lizard (Uta stansburiana) as a model, we examined how reproductive investment (clutch size and mass) influenced maternal immunological (BKA) and oxidative state (ROMs) and whether these metrics covaried with egg yolk immunity and oxidative state. We assessed factors influencing variation in egg yolk BKA and ROMs within and across clutches from all females and found that females with smaller clutches had higher BKA and ROMs than females with larger clutches. There was also an overall positive relationship between maternal BKA and ROMs and clutch mass, regardless of clutch size. We did not find maternal and egg yolk BKA and ROMs to be directly related, but yolk ROMs decreased as egg mass increased. Within-clutch variation in yolk BKA and ROMs was not related to maternal investment, but variation among clutches was explained by maternal identity. Because egg yolk physiology can impose long-lasting or permanent changes to offspring, these results create a foundation for future work investigating factors contributing to yolk physiology and highlight the necessity of considering multiple physiological and ecological variables when conducting eco-immunological research.

Seasonal reproductive allocation in landlocked Alewife Alosa pseudoharengus , in the context of niche construction and eco‐evolutionary feedbacks

The bidirectional dynamics between species and their biotic and abiotic environments, known as eco-evolutionary feedbacks, may shift the direction of evolution and alter the ecological role of species. Alewife, Alosa pseudoharengus, is an exemplary species to study reciprocal feedbacks between ecology and evolution, owing to repeated independent derivations of a landlocked life history from an ancestral anadromous form. In this study we analysed the reproductive allocation during the spawning season in a landlocked Alewife population in the context of eco-evolutionary feedbacks. We also compared our findings with previous results from a neighbouring anadromous population of the species. Similarities were found between the two Alewife populations in relation to their ovarian development, oocyte release strategy and fecundity type, but also differences in seasonal patterns of energy investment. Anadromous Alewives invested more in the size of the first oocyte batch of the season and subsequently tapered their reproductive allocation, while spawning batch in landlocked Alewife was invariant as the spawning season progressed. The evolutionary change from ancestral tapering to equitability of seasonal reproductive investment can be explained with reference to eco-evolutionary changes that occurred upon landlocking related to the availability of zooplankton prey and feeding opportunity.

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

Variation in nest building, aggression, learning, and steroid hormone levels in Betta splendens

Individuals within a population present behavioral responses that vary according to intrinsic and extrinsic factors such as ontogenetic phase, nutritional status, reproductive stage, and previous experiences. These differences can be explained by endogenous changes, such as hormone release, that can modulate reproductive behaviors, stress response, and cognitive processes. In order to investigate the relationship between behavior and hormonal levels in the fighting fish Betta splendens, the present study characterized nest building, aggressive behavior, learning of a task, and levels of cortisol and 11-ketotestosterone (11-KT) in 86 male Fighting fish. At the beginning of the experiment (days 1–4), fish were characterized as nest builders, intermediate builders, or non-builders. They were then sequentially tested for aggression (days 7–8), learning performance (days 11–21), and circulating hormone levels (day 23). Nest builders showed the lowest hormonal levels at the end of the experiment and low aggressiveness; Intermediate builders presented low cortisol, but high KT levels and best learned the task; Non-builders were the most aggressive animals with higher cortisol levels (at day 23). Our data suggest that in B. splendens, aggressive behavior and learning performance are related to the relative investment in reproduction and variation in circulating levels of corticosteroids and androgens.

Flight-Fecundity Trade-offs: A Possible Mechanistic Link in Plant-Herbivore-Pollinator Systems.

Plant–herbivore and plant–pollinator interactions are both well-studied, but largely independent of each other. It has become increasingly recognized, however, that pollination and herbivory interact extensively in nature, with consequences for plant fitness. Here, we explore the idea that trade-offs in investment in insect flight and reproduction may be a mechanistic link between pollination and herbivory. We first provide a general background on trade-offs between flight and fecundity in insects. We then focus on Lepidoptera; larvae are generally herbivores while most adults are pollinators, making them ideal to study these links. Increased allocation of resources to flight, we argue, potentially increases a Lepidopteran insect pollinator’s efficiency, resulting in higher plant fitness. In contrast, allocation of resources to reproduction in the same insect species reduces plant fitness, because it leads to an increase in herbivore population size. We examine the sequence of resource pools available to herbivorous Lepidopteran larvae (maternally provided nutrients to the eggs, as well as leaf tissue), and to adults (nectar and nuptial gifts provided by the males to the females), which potentially are pollinators. Last, we discuss how subsequent acquisition and allocation of resources from these pools may alter flight–fecundity trade-offs, with concomitant effects both on pollinator performance and the performance of larval herbivores in the next generation. Allocation decisions at different times during ontogeny translate into costs of herbivory and/or benefits of pollination for plants, mechanistically linking herbivory and pollination.

When Older Males Sire More Offspring—Increased Attractiveness or Higher Fertility?

In birds with extrapair mating, older males usually have higher fertilization success than younger males. Two hypotheses can potentially explain this pattern: 1) females prefer older, and often more ornamented males, or 2) older males invest more in reproduction and fertility than younger males. Here we studied factors associated with age-related male fertilization success in a population of barn swallows Hirundo rustica in Canada. We document that male fertilization success increased gradually up to a minimum age of four-year old. The age effect was especially strong for the number of extrapair offspring obtained and the occurrence of a second brood. The higher fertilization success of older males was also associated with an early start of breeding in spring. The length of the elongated outermost tail feathers, a postulated male ornament preferred by females, also increased with age (in both sexes), but it was not a significant predictor of male fertilization success within age classes. Male fertility traits, especially testis size, but also sperm motility and sperm velocity, increased significantly across age groups. Our results suggest that the higher fertilization success by older males is due to their higher reproductive investments and that their longer tails are an adaptation to early arrival on the breeding grounds.Significance statementThe barn swallow is a socially monogamous passerine with extensive extrapair mating. We found that males become more successful in siring both withinpair and extrapair offspring as they become older. Their increased fertilization success was associated with a higher reproductive effort as indicated by larger testes, more motile sperm, and an earlier start of breeding in spring. The length of the outer tail feathers increased with age in both sexes, but long tails did not enhance male fertilization success among males of the same age. Long tails are probably an adaptation to rapid migration and earlier arrival on the breeding grounds. Our findings suggest that the commonly observed age-related increase in male fertilization success in passerine birds is better explained by life history theory than by sexual selection theory.

Home range size and habitat quality affect breeding success but not parental investment in barn owl males

Life-history theory predicts that parents should balance their limited resources to maximize lifetime fitness, limiting their investment in current reproduction when the fitness value of current progeny is lower than that gained by producing offspring in the future. Here, we examined whether male barn owls (Tyto alba) breeding in low-quality habitats increased their parental effort to successfully complete offspring rearing or limited their investment by paying a fitness cost while saving energy for the future. We equipped 128 males with GPS devices between 2016 and 2020 to collect information on home range size, habitat composition, food provisioning rate to the brood and nightly distances covered. We also recorded nestlings’ growth and survival, as well as males’ body mass variation and future reproductive success. Males living in lower-quality habitats exploited bigger home ranges compared to individuals whose nests were settled in prey-rich habitats. They fed their brood less frequently, while covering longer nightly distance, resulting in a slower growth of late-hatched nestlings and ultimately in a lower fledging success. As males did not differ in body mass variation or future reproductive success our findings suggest that males hunting in home ranges with less prey-rich structures do not jeopardize future reproduction by investing disproportionately larger resources to compensate for their current low home range quality.

Salinity effects on the germination and reproduction of Eryngium maritimum L. (Apiaceae)

Coastal ecosystems are globally threatened. As sea level rises, flooding, salt-water intrusion and coastal regression are dramatically changing their environmental conditions. Eryngium maritimum L. (Apiaceae) mainly inhabits white dunes of the Mediterranean and Atlantic coasts. The present study aimed to analyse the effect of salinity on the germination and reproduction of the species. Seeds from Mallorca (Spain) were germinated with four different salts (NaCl, Na2SO4, MgCl2, MgSO4) at concentrations ranging from 0 to 0.4 M. On the other hand, seedlings were grown and watered with different seawater (SW) concentrations ranging from 6.25% SW to full SW. Reproductive investment was assessed considering the number of inflorescences, fruit set and seed set per plant per whorl in the different treatments. Complementarily, field electrical conductivity measurements were carried out in a natural population to assess its variability along the dune. Germination was inhibited by salts, with nearly null germination at concentrations higher than 0.1 M, with significant differences among salts. Specifically, Na2SO4 and MgCl2 strongly affected germination rather than NaCl and MgSO4. Plant dieback increased in concentrations higher than 50% SW. Fruit and seed production was inhibited by the presence of salts even at concentrations of 12.5% SW. Embryonic dune was the most saline area, with decreasing electrical conductivity in white and semi-fixed dunes. These results suggest that E. maritimum can deal with high salt concentrations along its life cycle. However, to germinate and reproduce, it tolerates only low salt concentrations. So, it should be considered as a halotolerant species. Considering its distribution along the dune, the salinity of the strandline could be, along with other factors, responsible for its decrease in fitness in front dunes. As a result of sea-level rise and coastal salinization, it can be hypothesized that the optimal distribution of E. maritimum along the dune will change, shifting from actual foredunes to dune-crests.

Sperm morphology and testicular histology of the polyandric species Leptodactylus podicipinus (Anura: Leptodactylidae) from an urban environment.

Anurans have a high reproductive diversity, which is closely associated with testicular dynamics and sperm production. This variety in reproduction is modulated by the sexual characteristics of reproductive strategies, such as polyandry. Leptodactylus podicipinus has high reproductive plasticity, wide geographical distribution, and polyandric behavior. Although aspects of the testes and sperm of this species are known, knowledge about the relationship between these aspects and reproductive investment is scarce. The present study evaluated the morphological characteristics of the testes and sperm in an urban environment. We used 11 sexually mature males from the city of Campo Grande, Mato Grosso do Sul, Brazil. The specimens were obtained from night excursions between April and September, the months that constitute the post-rainy season. The biometric data (snout-vent length, testes, and body mass) were associated with sperm parameters (length of the spermatozoon head and tail). Stereological analyses of sperm morphology and the testes were performed. The results showed correlations between testis mass and spermatozoon length, which were positively related to head length and negatively related to tail length. The locular area and tail length were also negatively correlated. The percentage of normal spermatozoa was 97%; however, some sperm heads and tails exhibited different morphologies from the pattern described for the species. The germinative structure comprised more than 50% of the locular area composed of spermatozoa. The results of this study contribute to the knowledge of aspects related to the reproductive biology of L. podicipinus obtained from an urban environment.

Nutrients Regulate the Effects of Arbuscular Mycorrhizal Fungi on the Growth and Reproduction of Cherry Tomato.

Arbuscular mycorrhizal fungi (AMF) colonize the rhizosphere of plants and form a symbiotic association with plants. Mycorrhizal symbionts have diversified ecological roles and functions which are affected by soil conditions. Understanding the effects of different AMF inoculation on plants under varied nutritional conditions is of great significance for further understanding the effects of the external environment regulating mycorrhizal symbiosis on plant phenotypic traits. In this study, the effects of four AMF inoculation treatments on the growth and reproductive performance of cherry tomato (Solanum lycopersicum var. cerasiforme) were investigated under three nutrient levels by pot experiment. It was found that the growth-promoting effect of AMF on cherry tomato decreased with nutrient reduction, and the effects of the same AMF inoculation treatment on cherry tomato were different at different nutrient levels. Nutrient levels and AMF had interactive effects on flower characteristics, fruit yield, resource allocation, and seed germination of the cherry tomato. In addition, AMF could promote sexual reproductive investment. Nutrient levels and AMF also affected the accumulation of nitrogen and phosphorus in cherry tomato, and there were significant differences among different AMF inoculation treatments. The results indicated that nutrient differences could affect the symbiosis between AMF and plants, and confirmed that there were differences in the effects of the four AMF inoculation treatments on the growth and reproductive traits of plants. The differences in growth and reproduction characteristics of cherry tomato between different AMF inoculation treatments at different nutrient levels indicated that the effects of AMF mycorrhizal on the traits of cherry tomato were regulated by nutrients.

Decades of warming alters maturation and reproductive investment in fish

Decades of warming alters maturation and reproductive investment in fish

The developmental high wire: Balancing resource investment in immunity and reproduction.

The strategic allocation of resources into immunity poses a unique challenge for individuals, where infection at different stages of development may result in unique trade‐offs with concurrent physiological processes or future fitness‐enhancing traits. Here, we experimentally induced an immune challenge in female Gryllus firmus crickets to test whether illness at discrete life stages differentially impacts fitness. We injected heat‐killed Serratia marcescens bacteria into antepenultimate juveniles, penultimate juveniles, sexually immature adults, and sexually mature adults, and then measured body growth, instar duration, mating rate, viability of stored sperm, egg production, oviposition rate, and egg viability. Immune activation significantly impacted reproductive traits, where females that were immune challenged as adults had decreased mating success and decreased egg viability compared to healthy individuals or females that were immune challenged as juveniles. Although there was no effect of an immune challenge on the other traits measured, the stress of handling resulted in reduced mass gain and smaller adult body size in females from the juvenile treatments, and females in the adult treatments suffered from reduced viability of sperm stored within their spermatheca. In summary, we found that an immune challenge does have negative impacts on reproduction, but also that even minor acute stressors can have significant impacts on fitness‐enhancing traits. These findings highlight that the factors affecting fitness can be complex and at times unpredictable, and that the consequences of illness are specific to when during an individual's life an immune challenge is induced.

Tibetan birds lay larger but fewer eggs in a clutch.

How do offspring size and number vary along elevational gradients? This is a striking but rarely addressed question in life-history evolution. Here we comparatively explore it using phylogenetically paired passerine birds of lowland China vs. the Tibetan plateau spanning an elevational range of 18-4500m. Toward the Tibetan plateau, egg size increased, clutch size decreased and total clutch volume (= clutch size × egg size) did not change, when accounting for major confounding factors. Larger eggs and smaller clutches can be a response to harsh abiotic conditions at higher elevations and the corresponding reduction in food resources required for raising young, respectively. There was a negative correlation between egg size and clutch size after controlling for elevation effect on either trait, suggesting that the trade-off contributed to the expression of these two traits across elevations, given the lack of an elevational trend in total clutch volume. Tibetan birds had a shorter breeding season, prolonged incubation and nestling period than their lowland counterparts. While fewer clutches over the short breeding season may facilitate the increase in egg size, the concentration of annual reproductive investment did not seem to act on clutch size; despite the smaller clutches, hard environments may impose greater costs of parental care on Tibetan birds. The current research provides insight into the evolution of avian life histories across elevations.

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.