Survival costs of reproduction predict age-dependent variation in maternal investment

Life-history theory predicts that older females will increase reproductive effort through increased fecundity. Unless offspring survival is density dependent or female size constrains offspring size, theory does not predict variation in offspring size. However, empirical data suggest that females of differing age or condition produce offspring of different sizes. We used a dynamic state-variable model to determine when variable offspring sizes can be explained by an interaction between female age, female state and survival costs of reproduction. We found that when costs depend on fecundity, young females with surplus state increase offspring size and reduce number to minimize fitness penalties. When costs depend on total reproductive effort, only older females increase offspring size. Young females produce small offspring, because decreasing offspring size is less expensive than number, as fitness from offspring investment is nonlinear. Finally, allocation patterns are relatively stable when older females are better at acquiring food and are therefore in better condition. Our approach revealed an interaction between female state, age and survival costs, providing a novel explanation for observed variation in reproductive traits.     

Evolutionary ecology of egg size and number in a seed beetle: genetic trade-off differs between environments

Abstract In many organisms, large offspring have improved fitness over small offspring, and thus their size is under strong selection. However, due to a trade-off between offspring size and number, females producing larger offspring necessarily must produce fewer unless the total amount of reproductive effort is unlimited. Because differential gene expression among environments may affect genetic covariances among traits, it is important to consider environmental effects on the genetic relationships among traits. We compared the genetic relationships among egg size, lifetime fecundity, and female adult body mass (a trait linked to reproductive effort) in the seed beetle, Stator limbatus , between two environments (host-plant species Acacia greggii and Cercidium floridum ). Genetic correlations among these traits were estimated through half-sib analysis, followed with artificial selection on egg size to observe the correlated responses of lifetime fecundity and female body mass. We found that the magnitude of the genetic trade-off between egg size and lifetime fecundity differed between environments–a strong trade-off was estimated when females laid eggs on C. floridum seeds, yet this trade-off was weak when females laid eggs on A. greggii seeds. Also differing between environments was the genetic correlation between egg size and female body mass–these traits were positively genetically correlated for egg size on A. greggii seeds, yet uncorrelated on C. floridum seeds. On A. greggii seeds, the evolution of egg size and traits linked to reproductive effort (such as female body mass) are not independent from each other as commonly assumed in life-history theory.     

Phenotypic variation in the breeding phenology of the woodlouse Armadillidium vulgare

Summary The breeding phenology of temperate wood-lice is strongly seasonal, the result of physiological constraints and precise environmental cues for reproduction. The adaptive value of such mechanisms is that the release of offspring coincides with favourable conditions for growth and survival (Willows 1984). We recorded the breeding phenology of Armadillidium vulgare (Latreille) on two grassland sites in Great Britain and found between-site and between-year variation in the onset of reproduction, the duration of reproductive activity, the release of offspring, the size of reproductive females and the number of broods per female. Between 82.7 and 97.7% of gravid females sampled were semelparous at 23 months, with the remainder iteroparous, producing a second brood after 35 months. On one site (Weeting Health) improved growth conditions during 1984 allowed some females (19.3% of gravid females sampled in that year) to produce a brood after 11 months. There was also an increase in the number of 3-year-old females found to be gravid. An experimental manipulation of the same habitat confirmed that such changes in life history tactics could be phenotypic responses. The observed phenotypic variation was sufficient to produce a range of life history tactics within a population. Mixtures of life history tactics within a population may be typical of invasive species and populations at the edge of the species range. Our results support the idea that phenotypic plasticity can be an appropriate tactic to maximise fitness in a fluctuating environment (Caswell 1983, 1989).     

Factors affecting variation in the reproductive investment of female treefrogs,Hyla intermedia

In anurans, fecundity (clutch size) is the most important determinant of female reproductive success. We investigated three possible causes responsible for fecundity variation in female Italian treefrogs, Hyla intermedia, during four breeding seasons: (i) variation in morphological (body size and condition) and life-history (age) traits; (ii) variation in the tradeoff between the number and the size of eggs; (iii) seasonal effects and within-season differences in the timing of deposition. At the population level, we found no evidence for a tradeoff between the number and the size of eggs, because they both correlated positively with females’ body size. Conversely, neither age nor post-spawning body condition showed any effect on female reproductive investment. Independent of body size, we found no evidence for variation in reproductive effort among different breeding seasons, but strong evidence for a decrease of clutch size and an increase of egg size with the advancing of a breeding season. To test for the functional significance of the observed temporal variation in allocation strategy, we carried out a rearing experiment in semi-natural conditions on a random sample of ten clutches. The experiment showed a negative effect of clutch size and a positive effect of egg size on both tadpole growth and developmental rates, suggesting that reproductive investment, although constrained by body size, can be adjusted by females to the time of deposition to increase the chances of offspring survival.     

Rain,prey and predators: climatically driven shifts in frog abundance modify reproductive allometry in a tropical snake

To predict the impacts of climate change on animal populations, we need long-term data sets on the effects of annual climatic variation on the demographic traits (growth, survival, reproductive output) that determine population viability. One frequent complication is that fecundity also depends upon maternal body size, a trait that often spans a wide range within a single population. During an eight-year field study, we measured annual variation in weather conditions, frog abundance and snake reproduction on a floodplain in the Australian wet-dry tropics. Frog numbers varied considerably from year to year, and were highest in years with hotter wetter conditions during the monsoonal season (“wet season”). Mean maternal body sizes, egg sizes and post-partum maternal body conditions of frog-eating snakes (keelback, Tropidonophis mairii, Colubridae) showed no significant annual variation over this period, but mean clutch sizes were higher in years with higher prey abundance. Larger females were more sensitive to frog abundance in this respect than were smaller conspecifics, so that the rate at which fecundity increased with body size varied among years, and was highest when prey availability was greatest. Thus, the link between female body size and reproductive output varied among years, with climatic factors modifying the relative reproductive rates of larger (older) versus smaller (younger) animals within the keelback population.     

Male genotype influences female reproductive investment in Drosophila melanogaster

In many species, males can influence the amount of resources their mates invest in reproduction. Two favoured hypotheses for this observation are that females assess male quality during courtship or copulation and alter their investment in offspring accordingly, or that males manipulate females to invest heavily in offspring produced soon after mating. Here, we examined whether there is genetic variation for males to influence female short-term reproductive investment in Drosophila melanogaster, a species with strong sexual selection and substantial sexual conflict. We measured the fecundity and egg size of females mated to males from multiple isofemale lines collected from populations around the globe. Although these traits were not strongly influenced by the male's population of origin, we found that 22 per cent of the variation in female short-term reproductive investment was attributable to the genotype of her mate. This is the first direct evidence that male D. melanogaster vary genetically in their proximate influence on female fecundity, egg size and overall reproductive investment.     

Cascading costs of reproduction in female house wrens induced to lay larger clutches

In many species, females produce fewer offspring than they are capable of rearing, possibly because increases in current reproductive effort come at the expense of a female's own survival and future reproduction. To test this, we induced female house wrens (Troglodytes aedon) to lay more eggs than they normally would and assessed the potential costs of increasing cumulative investment in the three main components of the avian breeding cycle – egg laying, incubation and nestling provisioning. Females with increased clutch sizes reared more offspring in the first brood than controls, but fledged a lower proportion of nestlings. Moreover, nestlings of experimental females were lighter than those of control females as brood size and prefledging mass were negatively correlated. In second broods of the season, when females were not manipulated, experimental females laid the same number of eggs as controls, but experienced an intraseasonal cost through reduced hatchling survival and a lower number of young fledged. Offspring of control and experimental females were equally likely to recruit to the breeding population, although control females produced more recruits per egg laid. The reproductive success of recruits from broods of experimental and control females did not differ. The manipulation also induced interseasonal costs to future reproduction, as experimental females had lower fecundity than controls when breeding at least 2 years after having their reproductive effort experimentally increased. Finally, females producing the modal clutch size of seven eggs in their first broods had the highest lifetime number of fledglings.     

It is time to mate: population-level plasticity of wild boar reproductive timing and synchrony in a changing environment

On a population level, individual plasticity in reproductive phenology can provoke either anticipations or delays in the average reproductive timing in response to environmental changes. However, a rigid reliance on photoperiodism can constraint such plastic responses in populations inhabiting temperate latitudes. The regulation of breeding season length may represent a further tool for populations facing changing environments. Nonetheless, this skill was reported only for equatorial, nonphotoperiodic populations. Our goal was to evaluate whether species living in temperate regions and relying on photoperiodism to trigger their reproduction may also be able to regulate breeding season length. During 10 years, we collected 2,500 female reproductive traits of a mammal model species (wild boar Sus scrofa) and applied a novel analytical approach to reproductive patterns in order to observe population-level variations of reproductive timing and synchrony under different weather and resources availability conditions. Under favorable conditions, breeding seasons were anticipated and population synchrony increased (i.e., shorter breeding seasons). Conversely, poor conditions induced delayed and less synchronous (i.e., longer) breeding seasons. The potential to regulate breeding season length depending on environmental conditions may entail a high resilience of the population reproductive patterns against environmental changes, as highlighted by the fact that almost all mature females were reproductive every year.     

Female reproductive biology of the sand smelt in brackish lagoons of southern France

The breeding season of Atherina boyeri living in the brackish lagoons of Mauguio, Pérols and Méjean (Hérault, southern France) was very protracted (February-September). The peak of the reproductive effort occurred in April, May and June. Larger fishes started spawning earlier, and stopped later, than smaller ones. Batch fecundity varied from 4 to 447 oocytes and was positively related to female length and weight. Monthly mean fecundity increased at the beginning of the breeding season and decreased between June and July. Individual mean oocyte diameter ranged from 1.34 to 1.94 mm and was not related to fish length. Monthly mean oocyte size declined throughout the breeding season as water temperature rose. There was no trade-off between number and egg size. The strategy of these sand smelts seemed well adapted to ensure spawning success without endangering their survival. The highest reproductive effort period occurred in such a way that environmental conditions were suitable to the best survival and growth of hatched larvae. When breeding ceased, fishes, particularly the youngest ones, had enough time to improve their condition before overwintering.     

Geographic variation of body size and reproductive patterns in Continental versus Mediterranean asp vipers, Vipera aspis

The occurrence of variation in body size and reproductive traits of Vipera aspis was assessed by analysing 74 reproductive females of different populations, collected throughout a large part of the distribution range of the taxon, from central‐western France to central Italy. Six populations were analysed, two of plain habitats, in France and Italy, characterized by a Continental climate, whereas the other four derived from two coastal and two inland, hilly Italian habitats, respectively, showing a Mediterranean climate. Females of the French area showed the smallest mean body size, whereas the pre‐ and post‐partum body masses of females from the coolest, central Italic area were significantly higher. Litter size varied among habitats and was significantly correlated with maternal body size. If the snout–vent length feature varied largely among offspring of different habitats (with the longest size occurring in representatives of the coastal, central Italian area), the average of both body mass and total mass of offsprings did not exhibit any clear pattern among populations colonizing different habitats. Nevertheless, relative litter mass was higher in the French continental populations, and lower in the coolest, Mediterranean, Italian ones. It is worth emphasizing the positive correlation between the snout–vent length feature of females and the total litter mass to environmental factors, such as hottest month temperature and total rainfall. The available literature records that female body size affects offspring size and fecundity. If the present study bolsters this correlation, it also rules out any other effect of female body size on the offspring characteristics analysed. Finally, evidence is provided for the role of climatic factors on life‐history traits (e.g. pre‐partum body mass) of asp vipers, although confounding effects pursued, for example, by food availability may occur. © 2009 The Linnean Society of London, Biological Journal of the Linnean Society, 2009, 96 , 383–391.     

Testing generalizations about latitudinal variation in reproduction and recruitment patterns with sicyoniid and caridean shrimp species

Summary

Study of latitudinal variation in seasonality of reproduction and recruitment of benthic marine invertebrates is useful in generating and testing hypotheses about causal factors acting on reproduction such as temperature and larval food supply that might be altered by changes in world climate. Analysis of latitudinal variation in reproductive patterns might be made with comparisons (a) among species with a common phylogenetic history from different latitudes and habitats and (b) among phylogenetically different taxa from the same location. Hypotheses on variation of reproductive seasonality with latitude are tested here with results of a study on nine species of caridean and two species of sicyoniid shrimp sampled from a tropical seagrass meadow in Puerto Rico. Breeding condition was determined by the presence or absence of incubated embryos (carideans) and the state of ovarian development in both carideans and sicyoniids. Recruitment was estimated from the percentage of individuals of monthly population samples in the juvenile size classes. Comparison of reproductive patterns among tropical, subtropical, and cool temperate Sicyonia spp. supports the paradigm of continuous reproduction in the tropics with increased restriction of breeding season with an increase in latitude. A greater intensity of breeding effort appears to accompany the shorter breeding period associated with an increase in latitude. At the tropical site most females of all caridean species carried embryos during all months of the year. With the onset of sexual maturity, caridean females produced consecutive broods for the rest of their relatively short (< 6 month) life span. In both sicyoniid and caridean species, recruitment occurred throughout the year but was highly variable, i.e., episodic rather than truly continuous or seasonal. Patterns of recruitment were highly concordant among but not between sicyoniid and caridean species, indicating that different sets of environmental factors controlled recruitment in the two groups. It is suggested that simultaneous study of adult reproduction and larval ecology is necessary to understand patterns of reproduction and recruitment. Coordinated effort on a global scale in studying latitudinal variation in reproduction and recruitment is suggested in order to predict the consequences of climate change on commercially and ecologically important marine invertebrate species.     

Breeding phenology in relation to NDVI variability in free-ranging African elephant

The phenology of reproduction is often correlated with resource availability and is hypothesized to be shaped by selective forces in order to maximize lifetime reproductive success. African elephants have the distinctive life history traits of a 22 month gestation and extended offspring investment, necessitating a long-term strategy of energy acquisition and reproductive expenditure to ensure successful offspring recruitment.
We investigated the relationship between the reproductive phenology of a wild elephant population and resource availability using remotely sensed Normalized Differential Vegetation Index (NDVI) data as a measure of time-specific primary productivity and hence forage quality.
The initiation of female elephants' 3+yr reproductive bout was dependent on conditions during the season of conception but timed so parturition occurred during the most likely periods of high primary productivity 22 months later. Thus, the probability of conception is linked to the stochastic variation in seasonal quality and the phenology of parturition is related to the predictable seasonality of primary productivity, indicating elephants integrate information on known current and expected future conditions when reproducing.
Juvenile mortality was not correlated with ecological variability, hence female fecundity rather than calf mortality appears to drive demographic processes in the study population.
Extreme climatic events, such as those associated with the El Niño-Southern-Oscillation (ENSO), acted to synchronize female fecundity in the population. This study suggests that the relationship between fecundity and ecological variability instigates the characteristic demographic fluctuations in elephant populations, rather than the mortality-driven fluctuations observed in many ungulate populations.     

Spatial and temporal variation in a suite of life-history traits in two species of wolf spider

Abstract.  1. Life-history traits and density were assayed in seven populations of two sympatric species of wolf spider for three consecutive years. The goal of the study was to quantify population dynamics and its relation to spatial and temporal life-history variation.
2. Adult female body size and fecundity varied significantly, among field sites and among years, in both species. Female spiders of both species differed in mean relative reproductive effort among sites, but not among years. The size of offspring was invariable, with no significant differences due to site or year.
3. All populations of both species tended to either decrease or increase in density during a given year and this was tightly correlated with changes in prey consumption rates.
4. Since life-history patterns are determined primarily by selection, it is concluded that size at sexual maturity for females is phenotypically plastic and responds to changes in prey availability. Offspring size however is not plastic and it is likely that other selection forces have determined offspring size. Temporal fluctuations in population size are correlated over a large area relative to dispersal capabilities for these species and conservation efforts for invertebrates must take this into consideration.     

Egg Size Versus Number of Offspring Trade-Off: Female Age Rather Than Size Matters in a Domesticated Arctic Charr Population

Understanding how organisms adjust reproductive allocation trade-offs between offspring size versus number (OSN trade-off) is a central question in evolutionary biology. In organisms with indeterminate growth, changes in OSN according to maternal size or age have been reported in numerous taxa. The relative contribution of age and size remains largely unclear, as they are often highly correlated. In this study, we investigated how females adjust the offspring size versus number trade-off and analyzed the relative contribution of female age and size in a domesticated population of Arctic charr Salvelinus alpinus (Linnaeus, 1758) that exhibit large variation in size within five age classes. Our results show that the reproductive output (i.e. as measured by the clutch mass), was strongly correlated to female mass and age suggesting that the proportion of resources allocated to reproduction do not vary along lifetime. Egg mass and fecundity (egg number) increased with female mass overall. However, within an age class, larger females had higher fecundity but egg mass was poorly related to female mass. At the population level, a positive relationship was observed between fecundity and egg mass but within each class age the relation was negative revealing a OSN trade-off. Overall, our results show that, in our model Arctic charr population, allocation trade-off to reproduction and the way females allocate to egg mass and fecundity is largely determined by their age rather than mass.     

Experimental manipulation of breeding density and litter size: effects on reproductive success in the bank vole

1. Reproductive success of individual females may be determined by density-dependent effects, especially in species where territory provides the resources for a reproducing female and territory size is inversely density-dependent.
2. We manipulated simultaneously the reproductive effort (litter size manipulation: ± 0 and + 2 pups) and breeding density (low and high) of nursing female bank voles Clethrionomys glareolus in outdoor enclosures. We studied whether the reproductive success (number and quality of offspring) of individual females is density-dependent, and whether females can compensate for increased reproductive effort when not limited by saturated breeding density.
3. The females nursing their young in the low density weaned significantly more offspring than females in the high density, independent of litter manipulation.
4. Litter enlargements did not increase the number of weanlings per female, but offspring from enlarged litters had lower weight than control litters.
5. In the reduced density females increased the size of their home range, but litter manipulation had no significant effect on spacing behaviour of females. Increased home range size did not result in heavier weanlings.
6. Mother's failure to successfully wean any offspring was more common in the high density treatment, whereas litter manipulation or mother's weight did not affect weaning success.
7. We conclude that reproductive success of bank vole females is negatively density-dependent in terms of number, but not in the quality of weanlings.
8. The nursing effort of females (i.e. the ability to provide enough food for pups) seems not to be limited by density-dependent factors.     

Population dynamics and reproductive aspects of Porcellio albinus (Isopoda,Oniscidea) of Zarat (Gabes,Tunisia)

Porcellio albinus is a nocturnal species inhabiting xeric habitats in Tunisia. Size distribution, population dynamics, breeding activity, fecundity, fertility, reproductive allocation (RA), and life span were studied to establish the reproductive strategy of a population of this species in the sandy coastal area of Zarat. Monthly sampling was undertaken between July 2012 and November 2013. The overall sex-ratio of P. albinus was female biased. The relative abundance of adults, much more representative than that of juveniles, might be the consequence of the absence of specimens less than 8 mm in size in all samples collected outside the burrows at night. Reproduction is seasonal in P. albinus with two breeding seasons, the first one from March to June and the second in September. Five cohorts were recruited per year, four during the spring and one during the fall. The number of eggs per female ranged from 13 to 67 and was positively correlated with female body size. Fertility varied from 5 to 39 mancae. Compared to other xeric species, RA was low to produce a brood, but high to release a single manca. The results provide a better understanding of the reproductive behavior of this terrestrial isopod, living under severe environmental conditions.     

Reproductive effort in viscous populations

Abstract.— Here I study a kin selection model of reproductive effort, the allocation of resources to fecundity versus survival, in a patch-structured population. Breeding females remain in the same patch for life. Offspring have costly, partial long-distance dispersal and compete for breeding sites, which become vacant upon the death of previous occupants. The main result is that the evolutionarily stable reproductive effort decreases as offspring dispersal rate increases. The result can be understood as follows: In a well-mixed population with global competition, neither adults nor juveniles compete with relatives, but in a patch-structured population with dispersal restricted to the juvenile phase, juveniles experience relatively less competition with relatives than adults, thus making juveniles relatively more valuable. Because this asymmetry between adults and juveniles decreases with the dispersal rate, so does the evolutionarily stable level of allocation to fecundity.     

Breeding success in cooperative meerkats: effects of helper number and maternal state

Studies of cooperatively breeding birds and mammals generallyconcentrate on the effects that helpers have on the number ofreproductive attempts females have per year or on the numberand size of offspring that survive from hatching/weaning toindependence. However, helpers may also influence breeding successbefore hatching or weaning. In the present study, we used anultrasound imager to determine litter sizes close to birth,and multivariate statistics to investigate whether helpers influencefemale fecundity, offspring survival to weaning, and offspringsize at weaning in cooperative meerkats, Suricata suricatta.We found that the number of helpers in a group was correlatedwith the number of litters that females delivered each year,probably because females in large groups gave birth earlierand had shorter interbirth intervals. In addition, althoughpup survival between birth and weaning was primarily influencedby maternal dominance status, helper number may also have asignificant positive effect. By contrast, we found no evidenceto suggest that helpers have a direct effect on either littersizes at birth or pup weights at weaning, which were both significantlyinfluenced by maternal weight at conception. However, becausedifferences in maternal weight were associated with differencesin helper number, helpers have the potential to influence maternalfecundity and offspring size within reproductive attempts indirectly.These results suggest that future studies may need to considerdirect and indirect helper effects on female fecundity and investmentbefore assessing helper effects on reproductive success in societiesof cooperatively breeding vertebrates.     

Larval population density affects female weight and fecundity in the dung beetle Aphodius ater

1. Competition for food at high densities during larval development leads to reduced adult weight in the northern temperate dung beetle Aphodius ater. 2. Analysis of female beetles caught in the field showed that numbers of eggs and total egg load per female were correlated positively with beetle size. 3. Female beetles reared at different population densities during larval development in the laboratory were analysed with regard to their lifetime fecundity and reproductive lifespan. 4. High population densities during development had a negative influence on the number of eggs per female and on reproductive lifespan. Lifetime fecundity was correlated positively with female weight. 5. It was concluded that competition during larval development in the first generation of offspring will result in a lower number of offspring in the second generation in Aphodius ater, and thereby reduce parental fitness.     

Size delays female senescence in a medium sized marsupial: The effects of maternal traits on annual fecundity in the northern brown bandicoot (Isoodon macrourus)

The degree to which females allocate resources between current reproduction, future fecundity and survival is a central theme in life history theory. We investigated two hypotheses proposed to explain patterns of reproductive investment, terminal investment and senescence, by examining the effects of maternal traits (age and maternal mass) on annual fecundity in female northern brown bandicoots, Isoodon macrourus (Marsupialia: Peramelidae). We found that annual fecundity in females declined in their final year of reproduction, indicating reproductive senescence. Maternal mass significantly influenced the rate of senescence and, in turn, a female's lifetime reproductive output. Mass had little effect on fecundity in 1st and 2nd year females, but a positive relationship with fecundity in 3rd year females. This meant that heavy, 3rd year females did not suffer the decline in fecundity shown in light 3rd year females. For 1st year females, mass and leg length increased between their first and second reproductive seasons, indicating a temporary shift, from the allocation of resources to reproduction, to increasing condition or structural size post their first breeding event. There were no net changes to body mass in subsequent years. We suggest that this year of post‐reproductive growth has important consequences for senescent effects on reproduction. Overall, results provided support for the effects of senescence on annual fecundity. Our findings were not consistent with the terminal investment hypothesis; reproductive output did not increase in females' final reproductive season despite a rapid decline in survival. However, this notion cannot be entirely dismissed; other measures of reproductive performance not examined here (e.g. offspring mass) may have provided an indication that females did increase their effort at the end of their lifespan. This study highlights the difficulty of measuring reproductive costs and the importance of understanding the combined effects of specific characteristics of an individual when interpreting reproductive strategies in iteroparous organisms.