Evolution of resource allocation between growth and reproduction in animals with indeterminate growth

We review the recent theoretical developments explaining the evolution of age-schedules of reproduction in animals with indeterminate growth. Indeterminate growth, i.e. growth that continues past maturation and may continue until the end of life, is characteristic for a large number of invertebrate taxa (e.g. clams, cladocerans and crayfish) and ‘lower’ vertebrate taxa (e.g. fish, amphibians, lizards and snakes). Many plants also exhibit indeterminate growth, and we liberally include studies focused on plants when they can be interpreted in terms of animal life histories. We focus on different measures used to determine the fittest life histories, on indeterminate growth as a problem of resource allocation and on the effects of environment to the evolution of the resource allocation schemes.     

Increased sperm allocation delays body growth in a protandrous simultaneous hermaphrodite

Sex allocation theory for simultaneous hermaphrodites predicts that hermaphrodites have a fixed amount of reproductive resources to allocate to both sex functions and that they trade off their allocation to both sexes depending on environmental conditions. Ophryotrocha diadema is a simultaneous hermaphroditic polychaete worm which has a protandrous phase prior to the hermaphroditic phase. The ability of adolescent males to compete with mature hermaphrodites for egg fertilization and the costs of an increase in male expenditure during the protandrous phase were tested in experiments where adolescent males had the possibility to fertilize hermaphrodites' eggs. Results document that adolescent males were able to compete with hermaphrodites for egg fertilization and caused the hermaphrodites fitness losses of 31.4%. Adolescent males which fertilized hermaphrodites' eggs had a slower growth rate than males which had no possibility to fertilize eggs. This result indicates that an increased male expenditure is a cost for adolescent males and that, during the protandrous phase, resources are allocated to reproduction at the expense of somatic development.  © 2003 The Linnean Society of London . Biological Journal of the Linnean Society , 2003, 78 , 149–154.     

Age, growth and reproduction of Cobitis paludica in a seasonal stream

In the Iberian endemic loach Cobitis paludica , in a small seasonal tributary of the Guadalquivir River, 65–70% of the total growth in length occurred in the first year of life. The maximum ages observed were 3+ years in males and 4+ years in females. Both sexes matured at the beginning of their second year of life. There was a significant difference from 1: 1 in the overall sex ratio of 412 males to 674 females. Spawning began in late March and ended in July. Cobitis paludica is a multiple spawner that releases a minimum of two batches of eggs per female each year. Once spawning had started, however, there was no recruitment from the stock of transparent oocytes to the mature stock. The number of eggs decreased from the first batch to the second, but there was no significant difference in the mean egg diameter between batches. Compared with other populations of this species, the present population, from a low latitude, is characterized by a low number of age groups, fast growth, early maturity and high fecundity in multiple spawnings. These life-history characteristics are typical of species in unstable environments, where adult mortality is high, variable or unpredictable.     

Mating frequency and resource allocation to male and female function in the simultaneous hermaphrodite land snail Arianta arbustorum

Sex allocation theory predicts that mating frequency and long‐term sperm storage affect the relative allocation to male and female function in simultaneous hermaphrodites. We examined the effect of mating frequency on male and female reproductive output (number of sperm delivered and eggs deposited) and on the resources allocated to the male and female function (dry mass, nitrogen and carbon contents of spermatophores and eggs) in individuals of the simultaneous hermaphrodite land snail Arianta arbustorum. Similar numbers of sperm were delivered in successive copulations. Consequently, the total number of sperm transferred increased with increasing number of copulations. In contrast, the total number of eggs produced was not influenced by the number of copulations. Energy allocation to gamete production expressed as dry mass, nitrogen or carbon content was highly female‐biased (>95% in all estimates). With increasing number of copulations the relative nitrogen allocation to the male function increased from 1.7% (one copulation) to 4.7% (three copulations), but the overall reproductive allocation remained highly female‐biased. At the individual level, we did not find any trade‐off between male and female reproductive function. In contrast, there was a significant positive correlation between the resources allocated to the male and female function. Snails that delivered many sperm also produced a large number of eggs. This finding contradicts current theory of sex allocation in simultaneous hermaphrodites.     

Annual cycle of energy allocation to growth and reproduction of yellow perch

Growth (length, weight) of yellow perch Perca flavescens in western and west-central Lake Erie began between June and July, possibly reaching asymptotic size by early winter. Energy density (kJ g⁻¹) of somatic tissue increased markedly from June to September, then declined to low levels by the following spring. Consequently, energy mass (kJ) of somatic tissue increased to September and then declined slowly until March. Ovarian growth began in October, and the size of the ovaries was maximal in April, just before spawning in May. The energy density of ovaries, however, increased to a peak in December, and then declined. The increase in ovary size in the winter, therefore, resulted largely from an allocation of tissue of low energy density. Fecundity and gonad size were correlated with somatic and gonadal energy density. A bioenergetics model was used to describe the monthly allocations of energy to respiration, growth, excretion, and reproduction. Most direct reproductive costs (80%) were incurred from September to December, corresponding to the cycle in the activity of the liver. Energy acquired in the early summer may be critical for determining maturation, fecundity, and egg quality. From 1978 to 1990, <80% of the females from the western and west-central basins of Lake Erie were classed as spent in July.     

Exposure to a novel male during late pregnancy influences subsequent growth of offspring during lactation

In mammals, allocation to reproduction can either be primed or suppressed in relation to cues from other individuals. Some conspecifics (e.g. potential mates) may enhance an individual's ability to reproduce but others may have a detrimental effect on reproductive success. One widely studied response to conspecific cues, the ‘Bruce effect’, occurs when pregnant females abort their pregnancies after exposure to a novel male. It has been suggested that this response has evolved as a counter‐tactic to the threat of infanticide posed by novel males. In some species, like mice, pregnancy termination will only occur if females are exposed to the unfamiliar male during a brief critical period early in pregnancy, which is surprising considering that an unfamiliar male threatens infanticide whenever present, and in particular near to birth. We demonstrate that female mice experiencing novel males during late pregnancy also alter their investment in progeny, but in a more subtle manner than previously observed. Females exposed to an unfamiliar male during late pregnancy give birth to offspring of a comparable weight to those produced by females exposed to the paternal male, but these offspring grow more slowly over lactation. As a consequence, offspring from these females weigh less at weaning. Modification of their growth trajectory, however, allows these offspring to catch up to normal weights by adulthood. Thus, cues of unfamiliar males, and possibly their associated threat of infanticide, can produce more wide‐ranging effects on maternal investment than previously recognized.     

Optimal individual growth and reproduction in perennial species with indeterminate growth

Summary A model predicting optimal timing of growth and reproduction in perennial species with indeterminate growth living in a seasonal environment, is presented. According to the model, the optimal fraction of growing season devoted to growth decreases with increasing individual age and size, which leads to S-shaped growth curves. Winter mortality seems to be a crucial factor affecting the timing of growth and reproduction, under the same function describing the dependence of growth rate and reproductive rate on body size. When winter mortality is heavy, it is often optimal to start reproducing in the first year, and to devote a large proportion of the subsequent years to reproduction, thus leading to small adult body sizes.The model has been applied to two species of mollusc and one species of fish. The model predictions fit well to the field data for these three species.     

羊草种群能量生殖分配的研究

对羊草种群能量生殖分配规律研究表明,在羊草种群中,各构件热值的大小顺序为穗〉营养枝叶鞘〉生殖枝叶鞘〉营养枝叶〉营养枝茎〉生殖枝茎〉生殖枝叶〉凋落物;营养生长和生殖生长的能量分配比例的大小顺序为营养枝〉根茎〉凋落物〉生殖枝;各构件能量分配比例的季节动态也有差异,在羊草种群的生殖枝构件中,茎和叶鞘的分配比例较大,而穗和叶的能量分配比例较小。     

Relative allocation to horn and body growth in bighorn rams varies with resource availability

Males may allocate a greater proportion of metabolic resourcesto maintenance than to the development of secondary sexual characterswhen food is scarce, to avoid compromising their probabilityof survival. We assessed the effects of resource availabilityon body mass and horn growth of bighorn rams (Ovis canadensis)at Ram Mountain, Alberta, Canada over 30 years. The number ofadult ewes in the population tripled during our study, and theaverage mass of yearling females decreased by 13%. We used theaverage mass of yearling females as an index of resource availability.Yearling female mass was negatively correlated with the bodymass of rams of all ages, but it affected horn growth only duringthe first three years of life. Yearly horn growth was affectedby a complex interaction of age, body mass, and resource availability.Among rams aged 2–4 years, the heaviest individuals hadsimilar horn growth at high and at low resource availability,but as ram mass decreased, horn growth for a given body massbecame progressively smaller with decreasing resource availability.For rams aged 5–9 years, horn growth was weakly but positivelycorrelated with body mass, and rams grew slightly more hornfor a given body mass as resource availability decreased. Whenfood is limited, young rams may direct more resources to bodygrowth than to horn growth, possibly trading long-term reproductivesuccess for short-term survival. Although horn growth of olderrams appeared to be greater at low than at high resource availability,we found no correlation between early and late growth in hornlength for the same ram, suggesting that compensatory horn growthdoes not occur in our study population. Young rams with longerhorns were more likely to be shot by sport hunters than thosewith shorter horns. Trophy hunting could select against ramswith fast-growing horns.     

The growth, development and reproduction of a deep sea cumacean (Crustacea: Peracarida)

A single sample of over 1000 individuals of Leuconjonesi Bishop, 1982, taken at a depth of about 1500 m on the continental slope off Surinam, was studied. The carapace length of individuals in the first postmarsupial instar was already about half that of brooding females. Growth increments at early moults were of 20–25. Males reached the final morphological form in the sixth postmarsupial instar. A prepuberty moult was recognized between the third and fourth male instars. Females reached the preparatory stage in the fourth postmarsupial instar. Brooding condition occurred for the first time after the next moult. The brooding form could then alternate at successive moults with an inter-brood form, resembling the preparatory female, with small, non-overlapping oostegites. Preparatory and inter-brood females were morphologically separable; vitellogenesis was restricted to these instars. Broods were of 6–12 young. The individuals in each brood probably completed marsupial development, and were released, one by one. The copepod parasite Sphaeronella infested 10", of brooding-form females.     

The age, growth and reproduction of Chondrostoma polylepis willkommi in a seasonal stream in the Guadalquivir River basin (southern Spain)

The age, growth and reproduction of Chondrostoma polylepis willkommi , an endemic cyprinid from the Iberian Peninsula, was studied for 2 years in a seasonal stream in the Guadalquivir River basin. Annual growth was low. Maximum ages observed were 5+ in males and 7+ in females. There was no significant difference in growth between sexes. Seasonal growth period started in May and continued for 2 to 6 months depending on age. The mean lengths of 1 + and 2+ age-groups decreased once the growth period had finished, probably related to reproductive stress and adverse ecological conditions, and this could explain the occurrence of Rosa Lee's phenomenon. Both sexes matured at the end of their second year of life (1+). There was a significant difference from 1: 1 in the overall sex ratio of 334 males to 464 females. Reproductive period started in March and lasted until May. Ch. p. willkommi was a multiple spawner that released two batches of eggs per female each year. The regression between fecundity ( F ) and fork length (l., mm) was: F =6.20 10³ L.^2.78. In females from age 2 + onwards, relative annual investment in somatic growth and reproduction was equivalent, implying that the same energy was allocated to reproduction as to maintenance/growth. Compared with other Ch. polylepis populations, the life-history patterns of this population, located in a small and seasonal stream in a southern latitude, were characterized by a low annual growth, a trade-off between reproduction and growth/maintenance, early maturity, low number of age-groups and high fecundity from multiple spawnings.     

Allometry and variability of resource allocation to reproduction in a wild reindeer population

The differential allocation of energy to either reproductionor survival represents a major conflict with important implicationsfor patterns of life history. Here, we explore how covariationbetween maternal body weight and fetal weight vary accordingto fetal sex in a wild reindeer (Rangifer tarandus) populationduring two contrasting years. Maternal weights differed duringthe 2 years, probably because of a difference in populationdensity. We could not detect any change in the allocation toreproduction depending on female phenotypic distribution. Malefetuses were heavier than female fetuses, with the same relativedimorphism in both years. There was no support for a correlationbetween the sex of the fetus carried by a female and her weight.Our results suggest that the level of resource allocation toreproduction during the prenatal period is strongly determinedby female body weight and the allometric relationship betweenbody weight and metabolic rate. We discuss the consequencesof our results for population dynamics. We call for an integrationof inter- and intraspecific allometric approaches to betterunderstand constraints and variation in life-history traits.     

Senescence in growth and reproductive allocation in a bunchgrass

• Senescence is a puzzling phenomenon. Few convincing studies of senescence in perennial herbaceous plants exist. While ramets are known to senesce, whether senescence of bunchgrasses actually occurs is not clear.
• In this study, we grew a set of plants of Elymus excelsus, a bunchgrass, to examine plant size, sexual reproduction and bud formation in individual plants in relation to their gradual ageing, in order to determine whether E. excelsus experiences senescence. We collected data in two consecutive years (2009 and 2010) from field samples of plants from 1 to 5 years old. Using regression models, we performed age‐related analyses of growth and reproduction parameters.
• Our results showed that individual plant size (diameter, individual biomass), total biomass of ramets, number and biomass of reproductive ramets, percentage of ramets that were reproductive, reproductive allocation, over‐wintering buds and juvenile ramets all declined with age. However, vegetative growth (number and biomass of vegetative ramets) did not decrease with age.
• Those plants that survived, dwindled in size as they aged. However, no plants shifted their resource allocation between growth and reproduction as they aged, so the shift in allocation did not account for the fall in size.

     

Life-history changes that accompany the transition from sexual to parthenogenetic reproduction in Drosophila mercatorum

In spite of the predicted genetic and ecological costs of sex, most natural populations maintain sexual reproduction, even those capable of facultative parthenogenesis. Unfertilized eggs from natural populations of Drosophila mercatorum occasionally develop into viable adults, but obligately parthenogenetic populations are unknown in this species. To evaluate the microevolutionary forces that both favor and constrain the evolution of parthenogenesis in D. mercatorum, we have measured parthenogenetic rates across a natural, sexually reproducing population and characterized the life-history changes that accompany the transition from sexual to parthenogenetic reproduction in laboratory strains. A highly significant difference in parthenogenetic rate was found between two populations in close geographic proximity, with increased rate found with lower population density. Laboratory strains of parthenogenetic females suffered increased mortality and reduced egg viability relative to their virgin counterparts from a sexual strain. Lifetime egg production was similar across all strains, but a shift in peak egg production to an earlier age also occurred. The combination of these life-history traits resulted in a higher net reproductive value for sexual females, but because they also had a longer generation time, intrinsic rate of increase was not as dramatically different from parthenogenetic females. In environments with high early mortality, there may be no fitness disadvantage to parthenogenesis, but the predicted ecological advantage of a twofold increase in intrinsic rate of increase was not realized. These results support the theory of Stalker (1956) that parthenogenesis is favored in environments in which sexual reproduction is difficult or impossible.     

Age structure, growth and reproduction of Leuciscus pyrenaicus in an intermittent stream in the Guadalquivir river basin, southern Spain

The age, growth and reproduction of Leuciscus pyrenaicus (Günther, 1868), an endemic cyprinid from the Iberian Peninsula, was studied from November 1987 to September 1989 in a small seasonal tributary of the Guadalquivir river basin. Maximum fork lengths observed were a 160 mm male with six scale annuli and a 171 mm female aged 7 +. Maximum ages observed were 7 + in males and 8 + in females. There were no significant differences in the annual growth increments between sexes. Seasonal growth period started in March and continued for 5 to 6 months. Mean lengths of 1 + specimens onwards diminished during summer and/or autumn. Males and females matured in their third and fourth year of life respectively. The overall sex ratio (272 males: 310 females) differed significantly from equality. Spawning began in May and ended in July. L. pyrenaicus is a multiple spawner that releases a minimum of two batches of eggs per female each year. Eggs in each batch were similar in both size (egg diameter) and number released. The relationship between fecundity (Fee) and fork length (mm) was represented by the formula: Fec=1.96 10⁻³ L^2.50.     

Life history evolution in Asobara tabida: plasticity in allocation of fat reserves to survival and reproduction

Life history variation can be genetically based, or it may be due to environmental effects on the phenotype. In this paper we examine life history variation in relation to differences in habitat in the parasitoid Asobara tabida. Differences in the spatial distribution of host patches, the length of the season, host suitability, and competition between parasitoids all contribute to the selection for differences in life history between strains from northern and southern Europe. Strains were compared with respect to the allocation between reproduction and survival in experimental environments that varied with regard to the availability of food or to the number of hosts offered per day. Upon emergence parasitoids originating from southern Europe have higher egg loads and smaller fat reserves than parasitoids originating from northern Europe. Parasitoids from both southern and northern Europe show plasticity in allocation: food shortage causes a decrease in egg production, and rich breeding opportunities an increase in egg production. This plasticity is greater in the northern strain. Fat reserves play a central role in the physiology of this allocation. Fat can be used for both reproduction and survival. There is no oosorption, so once fat is allocated to reproduction it can no longer be used for survival. Differences in plasticity in allocation can therefore be considered as differences in the timing of egg production.     

Resource allocation to growth,reproduction and survival in Gladiolus : The cost of male function

Theoretical models of life-history evolution assume trade-offs between present and future reproduction and/or survival. Models of the evolution of sex assume trade-offs between male function and female function. Generally, experiments designed to evaluate the cost of reproduction on other functions tend to ignore male function. The present work on Gladiolus takes into account simultaneously the different primary functions of the plant and separates sexual reproduction into one male component (pollen production) and one female component (seed production). The study of environmental (within-clone), between-clone and genetic correlations using strains of Gladiolus and principal component analysis show that trade-offs exist between male function, female function and survival, including both characters of plant vigour, perennation (corm production) and vegetative propagation (cormel production). Phenotypic correlations, using different species and species-hybrids, have been obtained which confirm these results. In particular, these results underline the importance of the impact of pollen production on the other functions.