Reproductive Investment Research Articles

How hibernation in frogs drives brain and reproductive evolution in opposite directions

Environmental seasonality can promote the evolution of larger brains through cognitive and behavioral flexibility but can also hamper it when temporary food shortage is buffered by stored energy. Multiple hypotheses linking brain evolution with resource acquisition and allocation have been proposed for warm-blooded organisms, but it remains unclear how these extend to cold-blooded taxa whose metabolism is tightly linked to ambient temperature. Here, we integrated these hypotheses across frogs and toads in the context of varying brumation (hibernation) durations and their environmental correlates. We showed that protracted brumation covaried negatively with brain size but positively with reproductive investment, likely in response to brumation-dependent changes in the socio-ecological context and associated selection on different tissues. Our results provide novel insights into resource allocation strategies and possible constraints in trait diversification, which may have important implications for the adaptability of species under sustained environmental change.

The Life-History Traits of Soil-Dwelling Nematode (Acrobeloides sp.) Exhibit More Resilience to Water Restriction Than Caenorhabditis elegans.

In the context of climate warming, the intensity and frequency of drought occurrences are progressively increasing. However, current research on the impacts of drought on the life-history traits and physiological activities of animals rarely encompasses soil animals that play crucial roles within soil ecosystems. Therefore, this study focused on a soil nematode species (Acrobeloides sp.) and a model nematode (Caenorhabditis elegans) to investigate whether nematodes adjust the trade-off of their life-history traits to confront arid environments, utilizing a Petri dish experiment. Subsequently, we assessed the resilience of the two nematode species to moisture variations by comparing the extent of changes in various indicators (i.e., life-history traits, physiological traits, and oxidative stress) of nematodes before and after drought and rehydration. The results revealed that both nematode species are capable of adapting to arid environments by altering the trade-off between life-history traits. Specifically, they reduce reproductive investment and body mass while maintaining life span, thus responding to drought conditions. Follow-up rehydration experiments post-drought stress highlighted that the soil-dwelling nematode exhibits a superior recovery capacity in response to moisture fluctuations in comparison to the model nematode. To the best of our knowledge, this is the first investigation into life history of drought adaptation within soil-dwelling nematodes. Moreover, the findings hold significant implications for the exploration of drought adaptation and its mechanisms in soil-dwelling animals.

Characterization of trade-offs between immunity and reproduction in the coral species Astrangia poculata.

Living organisms face ubiquitous pathogenic threats and have consequently evolved immune systems to protect against potential invaders. However, many components of the immune system are physiologically costly to maintain and engage, often drawing resources away from other organismal processes such as growth and reproduction. Evidence from a diversity of systems has demonstrated that organisms use complex resource allocation mechanisms to manage competing needs and optimize fitness. However, understanding of resource allocation patterns is limited across taxa. Cnidarians, which include ecologically important organisms like hard corals, have been historically understudied in the context of resource allocations. Improving understanding of resource allocation-associated trade-offs in cnidarians is critical for understanding future ecological dynamics in the face of rapid environmental change. Here, we characterize trade-offs between constitutive immunity and reproduction in the facultatively symbiotic coral Astrangia poculata. Male colonies underwent ex situ spawning and sperm density was quantified. We then examined the effects of variable symbiont density and energetic budget on physiological traits, including immune activity and reproductive investment. Furthermore, we tested for potential trade-offs between immune activity and reproductive investment. We found limited associations between energetic budget and immune metrics; melanin production was significantly positively associated with carbohydrate concentration. However, we failed to document any associations between immunity and reproductive output which would be indicative of trade-offs, possibly due to experimental limitations. Our results provide a preliminary framework for future studies investigating immune trade-offs in cnidarians.

Intraspecific divergence of sexual size dimorphism and reproductive strategies in a polytypic poison frog

AbstractIntraspecific variation in body size, both among populations and between sexes, is an important factor influencing life-history strategies. This variation might be the response to different environmental conditions, as well as natural and sexual selection, and can result in differences in behavior and reproductive strategies among populations. Here, we use the dyeing poison frog (Dendrobates tinctorius) as a model to investigate how interpopulation variation in body size and sexual size dimorphism affects reproductive strategies. As body size increased, sexual size dimorphism also increased, i.e., females were larger than males, and more so in populations with overall larger frogs. This indicates that there is a stronger selection for body size in females than in males, likely as a response to divergent reproductive investment between the sexes. Females from larger-bodied populations produced larger clutches, but the overall number of froglets produced per clutch did not differ among populations. We discuss potential causes and mechanisms that might be responsible for the observed divergence in body size, sexual size dimorphism, and reproductive strategies among populations that likely represent local adaptations. Our findings demonstrate the importance of cross-population studies, cautioning against drawing general conclusions about a species’ ecology without accounting for intraspecific variation.

Evolution of masting in plants is linked to investment in low tissue mortality

Masting, a variable and synchronized variation in reproductive effort is a prevalent strategy among perennial plants, but the factors leading to interspecific differences in masting remain unclear. Here, we investigate interannual patterns of reproductive investment in 517 species of terrestrial perennial plants, including herbs, graminoids, shrubs, and trees. We place these patterns in the context of the plants’ phylogeny, habitat, form and function. Our findings reveal that masting is widespread across the plant phylogeny. Nonetheless, reversion from masting to regular seed production is also common. While interannual variation in seed production is highest in temperate and boreal zones, our analysis controlling for environment and phylogeny indicates that masting is more frequent in species that invest in tissue longevity. Our modeling exposes masting-trait relationships that would otherwise remain hidden and provides large-scale evidence that the costs of delayed reproduction play a significant role in the evolution of variable reproduction in plants.

Maternal investment in arranged and self-choice marriages: A test of the reproductive compensation and differential allocation hypothesis in humans

The Reproductive Compensation (RC) hypothesis and the Differential Allocation (DA) hypothesis predict that parents who mate under constraint will either increase or decrease, respectively, their reproductive effort and investment in offspring. One possible type of mate choice constraint in humans is arranged marriage in which parents or others choose mates. To test the RC and DA hypotheses in humans, we examine whether there are differences in parental investment between women in arranged marriages and those in self-choice marriages using data from the Indonesian Family Life Survey (n = 8393). Marriage type does not significantly correlate with parental investment except for fertility outcomes where women in self-choice marriages had more live births, living children, and greater marital fertility than woman in arranged marriages. Our findings better support the DA hypothesis than the RC hypothesis. We conclude that, like many other species, free mate choice is associated with increased reproductive success in this sample of humans.

Predation Risk, and Not Shelter or Food Availability, as the Main Determinant of Reproduction Investment in Island Lizards

Reproductive investment, including the number of offspring produced, is one of the fundamental characteristics of a species. It is particularly important for island vertebrates, which face a disproportionate number of threats to their survival, because it predicts, among other things, a species’ resilience to environmental disruption. Taxa producing more offspring recover more quickly from environmental perturbations and survive environmental change better. However, ecologists do not understand which primary drivers shape a species’ reproductive investment well. Here, we compare the reproductive efforts of 14 island populations of the Aegean Wall Lizard (Podarcis erhardii), which lives across widely diverging environmental conditions. We test three hypotheses, namely that reproductive investment (measured as clutch size, clutch volume) is (1) positively associated with predation risk [‘Predation Risk Hypothesis’]; (2) positively associated with the presence of reliable vegetation cover that provides shelter [‘Gravid Female Protection Hypothesis’]; and (3) limited by (and hence positively correlated with) food availability [‘Food Limitation Hypothesis’]. Although field data are somewhat consistent with all three hypotheses, statistical analyses provide strong support for the Predation Risk Hypothesis. The results not only shed light on which fundamental forces shape reproductive investment in island vertebrates, but can also help shape conservation priorities.

Agricultural intensification affects birds' trait diversity across Europe

Agricultural intensification reduces the taxonomic diversity of bird communities, but its influence on functional diversity has been less studied. Here, we analyze the response of functional diversity of different cereal farmland bird communities across Europe to a gradient of agricultural intensification. We collected bibliographical information on life history traits (i.e. body mass, brain size, age of sexual maturity, clutch size, number of clutches, lifespan) of 30 species of birds recorded during field surveys in eight European countries. The index "brood value" was calculated to know each species’ level of reproductive investment per clutch. Intensification gradients at two spatial scales were obtained from field data through PCA, related to management practices at the field scale and the variation in structure and composition of farmland at the landscape scale respectively. We calculated the functional diversity index (FD) and the community-weighted mean (CWM) for each trait and sampling area, and linear mixed models in relation to the two intensification gradients were performed. Results showed that stronger intensification at the field level favors the assembly of shorter-lived communities and bird species with smaller relative brain sizes, also decreasing overall trait diversity. It also restricts the range of strategies for parental investment, reducing the functional diversity of the brood value index. More intensive field management would favor bird communities dominated by generalist and even introduced and/or managed hunting species, while putting at risk those farmland- and grassland-adapted species, typically more associated with the provision of ecosystem services. This highlights the relevance of field management (agrochemicals use, ploughing frequency) for the functional composition of bird communities and the conservation of farmland biodiversity. These findings add to existing knowledge on how species’ pace of life and cognitive capacity interact with drivers of global change, such as agricultural intensification.

Intensive sea urchin harvest rescales Paracentrotus lividus population structure and threatens self-sustenance.

The harvest of the edible sea urchin Paracentrotus lividus is intensively practiced in some regions of the Western Mediterranean Sea. The removal of the largest individuals can determine an overall reduction in population size and a size class truncation that can lead to a drastic drop the self-sustenance. The aim of this study is to evaluate the variability of the population reproductive potential across 5 years in one of the main harvest hotspots of Sardinia (Western Mediterranean Sea). The breeding stock consists of commercial and under-commercial size individuals which were sampled on a monthly basis to estimate their GonadoSomatic Index (GSI) and the Individual Gamete Output (IGO). In addition, the reproductive potential of the population-Total Gamete Output (TGO)-was calculated across the 5-year period in relation with the variation of the density of the breeding stock. During the last year, the reproductive potential was also estimated in a well-conserved population of a nearby Marine Protected Area. No significant variability in GSI and IGO was found over the 5 years nor when compared with the ones of protected population in the last year. However, the intensive harvest drastically rescaled the population body-size: although density of the commercial size class remained low, density of the under-commercial size-class halved from the beginning to the end of the study. Accordingly, the proportional decrease of their gamete output contribution led to a 40% loss of the reproductive potential of the whole population in the 5-year period. Interestingly, despite the loss of reproductive potential due to the decrease of the breeding stock density, the average values of IGO slightly increased across the years leading to the highest Annual Gamete Output (AGO) during the fourth year of sampling. This positive pattern could suggest a mechanism of reproductive investments of the survivors in terms of gonad production rate or increase in spawning intensity. This work provides evidence of the direct effect of size-selective harvesting on the rapid loss of population self-sustenance. Furthermore, it lays new prospective for future research of the indirect effects of the rescaling population body-size in functional traits of the sea urchin P. lividus and that could become important for both, sustainable exploitation and ecosystem conservation management.

Seasonality predicts variation in life history phenotypes in the livebearing fish Priapichthys annectens

Abstract Livebearing fishes (Poeciliidae) have been used as models to test several aspects of life history theory. Previous work in these fishes showed that traits such as age and size at maturity, reproductive allocation, and number and size of offspring can each be shaped by natural selection. Life history traits can also be influenced by the environment, and in some cases, such phenotypic plasticity can also be adaptive. Resource availability in the environment can affect life history trait expression with increased resources expected to result in increased investment in reproduction. Here, we test this hypothesis in the Costa Rican livebearing fish Priapichthys annectens by quantifying life history traits and comparing trait values between populations collected during the dry season versus the wet season, periods when resource availability varies. We found that life history traits related to reproductive investment, but not the timing of reproductive events, differed between seasons. During the wet season, female body condition increased, and females invested less in reproduction, having fewer but larger offspring. Irrespective of the season, larger females gave birth to larger offspring. Finally, we found that this species utilizes a lecithotrophic strategy of provisioning eggs with nutrients being deposited in the ova prior to fertilization, and that females only carry one developing brood at a time (no superfetation). This is the first study documenting the life history of P. annectens, and it adds to a growing body of work suggesting that seasonal environmental differences can induce changes in the expression of some—but not all—life history traits.

What counts as investment? Productive and unproductive expenditures

There have been significant changes in what economists include in the category of investment over the last six decades. The US government agency that compiles national income date, the Bureau of Economic Analysis, has tried to keep up with these changes, but it has not succeeded. The resulting tension between economic theory and official data can be overcome by adopting a different theoretical lens. Work on social reproduction and social investment suggests a more coherent definition of investment than that offered by mainstream economists. The paper then contrasts the measurement of investment in the government data with a calculation of investment derived from this new approach. The results show that business investment is dwarfed by the combined investment made by government and households. This finding suggests that business investment is not the key engine that powers the economy. This has significant implications for economic and social policies.

Preparing for the future offspring: European perch (Perca fluviatilis) biosynthesis of physiologically required fatty acids for the gonads happens already in the autumn.

Long-chain polyunsaturated fatty acids (PUFA) are critical for reproduction and thermal adaptation. Year-round variability in the expression of fads2 (fatty acid desaturase 2) in the liver of European perch (Perca fluviatilis) in a boreal lake was tested in relation to individual variation in size, sex, and maturity, together with stable isotopes values as well as fatty acids (FA) content in different tissues and prey items. ARA and DHA primary production was restricted to the summer months, however, perch required larger amounts of these PUFA during winter, as their ARA and DHA muscle content was higher compared to summer. The expression of fads2 in perch liver increased during winter and was higher in mature females. Mature females stored DHA in their gonads already in late summer and autumn, long before the upcoming spring spawning period in May. Lower δ13CDHA values in the gonads in September suggest that these females actively synthesized DHA as part of this reproductive investment. Lower δ13CARA values in the liver of all individuals during winter suggest that perch were synthesizing essential FA to help cope with over-wintering conditions. Perch seem able to modulate its biosynthesis of physiologically required PUFA in situations of stress (fasting or cold temperatures) or in situations of high energetic demand (gonadal development). Biosynthesis of physiologically required PUFA may be an important part of survival and reproduction in aquatic food webs with long cold periods.

Age-specific effects of density and weather on body condition and birth rates in a large herbivore, the Przewalski’s horse

Reproduction in young females can show a particularly sensitive response to environmental challenges, although empirical support from individual-based long-term studies is scarce. Based on a 20-year data set from a free-roaming Przewalski’s horse population (Equus ferus przewalskii), we studied effects of large-herbivore density (horses + cattle) and weather conditions experienced during different life stages on females’ annual birth rates. Foaling probability was very low in 2-year-olds, reaching maximum values in 5 to 10-year-olds, followed by a decrease in older females indicating reproductive senescence. Mother’s previous reproductive investment affected her current reproduction; young and old mothers (as opposed to middle-aged ones), which had nursed a foal for at least 60 days during the previous year, reproduced with a lower probability. Foaling probability and body condition of young females were lower when large-herbivore density was high. Reproduction was also influenced by interactive weather effects during different life stages. Low late-summer precipitation during the females’ year of birth was associated with a pronounced decrease in foaling probability in response to harsh late-winter temperatures prior to the mating season. In turn, increased amounts of late-summer rain during this early age together with more late-summer rain during the females’ current pregnancy led to an increased reproductive probability in 2–3-year-olds. These results were corroborated by the ameliorating effects of late-summer rain on body condition in such females. In conclusion, our findings highlight the interactive importance of weather conditions experienced during early life, and of density and weather during current pregnancy on foaling probability, particularly in young females.

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.

Video Transect-Based Coral Demographic Investigation

Demographic studies that quantify species’ performances for survival, growth, and reproduction are powerful means to characterize sources of demographic bottlenecks and predict community dynamics. However, they require fine-scale surveys of populations in the field, and are often too effort-intensive to be replicable at a large scale and in the long term. We developed a standardized digital approach for extracting demographic data on species’ abundances, sizes, and positions within video transects, enabling back-from-the-field data acquisition and therefore optimizing time spent in the field. The approach is based on manual species identification, size measurements, and mapping in video transects, mimicking what is traditionally performed in the field, though it can be automated in the future with the deployment of artificial intelligence. We illustrate our approach using video surveys of a reef-building coral community in New Caledonia. The results characterize the composition of the coral community and demographic performances as key ecological indicators of coral reef health, shed light on species’ life strategies and constraints to their demographics, and open paths for further quantitative investigations. Key findings include the diversity of life strategies with contrasting levels of investment in survival, growth, and reproduction found among the six taxa dominating the coral community (Acropora, Montipora, Porites, Galaxea, Favia, Millepora), indicating the diversity of demographic paths to ecological success. Our results also indicate that several species have adapted mechanisms to prevail under limiting hydrodynamic environments through the propagation of coral fragments. Our approach facilitates image-based demographic investigations, supporting endeavors in ecology and ecosystem management.

Supplemental oxygen does not improve growth but can enhance reproductive capacity of fish.

Fish tend to grow faster as the climate warms but attain a smaller adult body size following an earlier age at sexual maturation. Despite the apparent ubiquity of this phenomenon, termed the temperature-size rule (TSR), heated scientific debates have revealed a poor understanding of the underlying mechanisms. At the centre of these debates are prominent but marginally tested hypotheses which implicate some form of 'oxygen limitation' as the proximate cause. Here, we test the role of oxygen limitation in the TSR by rearing juvenile Galaxias maculatus for a full year in current-day (15°C) and forecasted (20°C) summer temperatures while providing half of each temperature group with supplemental oxygen (hyperoxia). True to the TSR, fish in the warm treatments grew faster and reached sexual maturation earlier than their cooler conspecifics. Yet, despite supplemental oxygen significantly increasing maximum oxygen uptake rate, our findings contradict leading hypotheses by showing that the average size at sexual maturation and the adult body size did not differ between normoxia and hyperoxia groups. We did, however, discover that hyperoxia extended the reproductive window, independent of fish size and temperature. We conclude that the intense resource investment in reproduction could expose a bottleneck where oxygen becomes a limiting factor.

Seasonal lipid dynamics of four Arctic bivalves: Implications for their physiological capacities to cope with future changes in coastal ecosystems.

The Arctic is exposed to unprecedented warming, at least three times higher than the global average, which induces significant melting of the cryosphere. Freshwater inputs from melting glaciers will subsequently affect coastal primary production and organic matter quality. However, due to a lack of basic knowledge on the physiology of Arctic organisms, it remains difficult to understand how these future trophic changes will threaten the long-term survival of benthic species in coastal habitats. This study aimed to gain new insights into the seasonal lipid dynamics of four dominant benthic bivalves (Astarte moerchi, Hiatella arctica, Musculus discors, and Mya truncata) collected before and after sea ice break-up in a high-Arctic fjord (Young Sound, NE Greenland). Total lipid content and fatty acid composition of digestive gland neutral lipids were analyzed to assess bivalve energy reserves while the fatty acid composition of gill polar lipids was determined as a biochemical indicator of interspecies variations in metabolic activity and temperature acclimation. Results showed a decrease in lipid reserves between May and August, suggesting that bivalves have only limited access to fresh organic matter until sea ice break-up. The lack of seasonal variation in the fatty acid composition of neutral lipids, especially essential ω3 fatty acids, indicates that no fatty acid transfer from the digestive glands to the gonads occurs between May and August, and therefore, no reproductive investment takes place during this period. Large interspecies differences in gill fatty acid composition were observed, which appear to be related to differences in species life span and metabolic strategies. Such differences in gill fatty acid composition of polar lipids, which generally influence metabolic rates and energy needs, may imply that not all benthic species will be equally sensitive to future changes in primary production and organic matter quality in Arctic coastal habitats.

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

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

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.

Plumage color degradation indicates reproductive effort: an experiment

Plumage color has traditionally been regarded as a static ornamental trait, but evidence is accumulating for significant color changes without molt that typically reduce the conspicuousness of ornamentation. In some species, the social partner seems to increase its reproductive investment if the color trait is experimentally enhanced, suggesting that color change could act as a signal. However, the information content of this signal is so far unclear. For example, birds in poor condition or making greater effort may deteriorate more severely. We used brood size manipulations to alter the reproductive effort of male and female collared flycatchers Ficedula albicollis. Both sexes showed less severe decline in some reflectance attribute of their white breast when their brood was experimentally reduced. In each sex, greater deterioration of the reflectance trait affected by the manipulation was accompanied by increased feeding rate by the partner. These feeding patterns do not prove, but are consistent with, a compensatory response by the partner to induced degradation. The manipulation effects on color change we detected confirm for the first time that plumage color deterioration can indicate current reproductive effort, thereby providing a potential fitness advantage to social partners that react to such deterioration.