Investment in survival and reproduction along a semelparity–iteroparity gradient in the Beta species complex

The Beta species complex shows a gradient of life histories from pronounced semelparity (big‐bang reproduction) to pronounced iteroparity (repeated reproduction). Models assume a trade‐off between investment in reproduction and survival. Reproductive effort is thought to increase with decreasing life span, and to be invariable in semelparous plants and susceptible to environmental conditions in iteroparous plants. These assumptions and hypotheses were verified by a greenhouse experiment testing six different life cycles at three contrasting nutrient levels. This study suggests that reproductive effort is negatively correlated with mean life span along the life‐cycle gradient. Unlike semelparous beets, reproductive effort in iteroparous beets is extremely sensitive to nutrient level. Phenotypic correlation between allocation to reproduction and allocation to survival generally appeared significantly negative in the longest‐lived iteroparous beets, nonsignificant in intermediate life histories and obviously positive in semelparous beets (no trade‐off control).     

Life history tactics of darters (Percidae: Etheostomatiini) and their relationship with body size, reproductive behaviour, latitude and rarity

Patterns of covariation of life history traits of darters in the genus Etheostoma are reviewed. The primary pattern is associated with body size. Large darters grow faster, mature at a larger size, produce bigger clutches, and have longer reproductive and life spans, and shorter spawning seasons, than do small darters. When the effects of size are removed statistically, the dominant secondary pattern matched the r-K continuum from fast-growing, short-lived, primarily semelparous species with many small ova and a high reproductive effort (r-species) to slow-growing, long-lived, iteroparous species with few large ova and a low reproductive effort (K-species). Variation in life history traits is also influenced by reproductive behaviour, latitude, and rarity (as measured by geographic range). There are significant differences in the primary and secondary life history patterns among reproductive guilds. Latitude and rarity are not correlated with these primary and secondary patterns. Instead, they account for variation of tertiary patterns. Rare species may not match the reproductive performance of more common and widely distributed species. Future studies of life history traits in darters should focus on species whose reproductive behaviour differs from that of the species reviewed in this study, and on the demographic characteristics of rare or declining populations.     

LIFE-HISTORY VARIATION WITHIN A POPULATION OF THE COLONIAL ASCIDIAN BOTRYLLUS SCHLOSSERI. I. THE GENETIC AND ENVIRONMENTAL CONTROL OF SEASONAL VARIATION

Many empirical analyses of life-history tactics are based on the assumption that demographic variation ought to be greatest among populations or species living in different environments. However, in a single population of the sessile colonial sea squirt Botryllus schlosseri, there are two discrete life-history morphs. Semelparous colonies are characterized by a) death immediately following the production of a single clutch, b) early age at first reproduction, c) rapid growth to first reproduction, and d) high reproductive effort. In contrast, iteroparous colonies a) produce at least three clutches before dying, b) postpone sexual reproduction until they are nearly twice the age of semelparous colonies, c) grow at about half the rate of semelparous colonies, and d) invest roughly 75% less in reproductive effort than semelparous colonies. Semelparous colonies numerically dominate the population through midsummer; later in the summer, iteroparous colonies are most numerous. Field and laboratory common-garden experiments, along with breeding studies, indicate that the demographic differences between the morphs are genetically determined. Consequently, the seasonal switch from dominance by semelparous colonies to dominance by iteroparous colonies may be an evolved response to a seasonally changing environment. On theoretical grounds, temporal variation in selection is thought to play a relatively unimportant role in maintaining genetic polymorphism; nonetheless, the seasonally recurrent life-history polymorphism shown in this study indicates that temporal variation in selection can lead to the maintenance of genetic polymorphism for traits strongly affecting fitness.     

The role of extreme iteroparity and risk avoidance in the evolution of mating systems

How much should a female be willing to risk in any one reproductive event? Highly iteroparous females will be risk averse and very conservative in their behaviour. Such females will be expected to avoid mortality risks and seek assurance that any current reproductive activity is safe. By way of minimizing risk, these same females will not engage in mate assessment or mate searching to the same degree as less iteroparous species, if these activities involve increased risk of mortality. Using a field experiment in a highly iteroparous species (the bluehead wrasse, Thalassoma bifasciatum ), it is shown that females in this species are indeed relatively risk averse. More importantly, the experiment also shows that individuals vary in their risk aversion depending on local population size, in a manner predicted from life-history theory. Then it is reviewed how several important aspects of the mating system in this species are best interpreted as results of conservative, risk-averse female behaviour. Finally, these ideas are generalized to suggest how basic aspects of the mating system might differ between species with many reproductive events over the lifetime (e.g. many tropical reef fishes) v. species with few reproductive opportunities (e.g. many temperate freshwater and marine fishes).     

Brood rearing costs affect future reproduction in the precocial common goldeneye Bucephala clangula

Life-history theory assumes a trade-off between current reproductive effort and future reproductive success. There are a large number of studies demonstrating reproductive trade-offs in different animal taxa, particularly in birds. Most bird studies have focused on the costs of chick rearing in altricial species. These costs have been assumed to be low in precocial species, but this aspect has been little studied. We used long-term individual reproductive data from the common goldeneye Bucephala clangula , an iteroparous precocial duck with uniparental female care, to examine whether brood rearing carries costs that affect future reproductive performance. All females were experienced breeders, and possible differences in female quality were ruled out. We compared within-individual (between-year) changes in clutch size, hatching date and body mass between females that had reared a brood in the previous year and females that had not. It turned out that brood rearing involved a cost in terms of clutch size and hatching date the next year, but not in terms of body mass: females that had reared a brood in the previous year laid relatively smaller clutches and laid relatively later than females that had not reared a brood. Our results show that normal brood rearing in a precocial species involves costs that affect future reproduction.     

Evolutionary demography of iteroparous plants: incorporating non-lethal costs of reproduction into integral projection models

Understanding the selective forces that shape reproductive strategies is a central goal of evolutionary ecology. Selection on the timing of reproduction is well studied in semelparous organisms because the cost of reproduction (death) can be easily incorporated into demographic models. Iteroparous organisms also exhibit delayed reproduction and experience reproductive costs, although these are not necessarily lethal. How non-lethal costs shape iteroparous life histories remains unresolved. We analysed long-term demographic data for the iteroparous orchid Orchis purpurea from two habitat types (light and shade). In both the habitats, flowering plants had lower growth rates and this cost was greater for smaller plants. We detected an additional growth cost of fruit production in the light habitat. We incorporated these non-lethal costs into integral projection models to identify the flowering size that maximizes fitness. In both habitats, observed flowering sizes were well predicted by the models. We also estimated optimal parameters for size-dependent flowering effort, but found a strong mismatch with the observed flower production. Our study highlights the role of context-dependent non-lethal reproductive costs as selective forces in the evolution of iteroparous life histories, and provides a novel and broadly applicable approach to studying the evolutionary demography of iteroparous organisms.     

A dynamic model of size-dependent reproductive effort in a sequential hermaphrodite: a counterexample to Williams's conjecture

In 1966, G. C. Williams showed that for iteroparous organisms, the level of reproductive effort that maximizes fitness is that which balances the marginal gains through current reproduction against the marginal losses to expected future reproduction. When, over an organism's lifetime, the value of future reproduction declines relative to the value of current reproduction, the level of effort allocated to current reproduction should always increase with increasing age. Conversely, when the value of future reproduction increases relative to the value of current reproduction, the level of effort allocated to current reproduction should decrease or remain at zero. While this latter pattern occurs commonly in species that exhibit a delayed age at first reproduction, it may also occur following an initial period of reproduction in some sex-changing organisms that experience a dramatic increase in reproductive potential as they grow larger. Indeed, this schedule of reproductive effort is predicted by models of "early" sex change; however, these models may arrive at this result incidentally because they consider only two reproductive states: on and off. In order to examine the schedule of reproductive effort in greater detail in a system where the potential reproductive rate increases sharply, we adapt the logic and methods of time-dependent dynamic-programming models to develop a size-dependent model of reproductive effort for an example species that experiences a dramatic increase in reproductive potential at large sizes: the bluehead wrasse, Thalassoma bifasciatum. Our model shows that the optimal level of reproductive effort will decline with increasing size or age when increases to the residual reproductive value outpace the increases to current reproductive potential. This result confirms the logic of Williams's analysis of optimal life histories, while offering a realistic counterexample to his conjecture of ever-increasing allocation to current reproduction.     

Between semelparity and iteroparity: Empirical evidence for a continuum of modes of parity

The number of times an organism reproduces (i.e., its mode of parity) is a fundamental life‐history character, and evolutionary and ecological models that compare the relative fitnesses of different modes of parity are common in life‐history theory and theoretical biology. Despite the success of mathematical models designed to compare intrinsic rates of increase (i.e., density‐independent growth rates) between annual‐semelparous and perennial‐iteroparous reproductive schedules, there is widespread evidence that variation in reproductive allocation among semelparous and iteroparous organisms alike is continuous. This study reviews the ecological and molecular evidence for the continuity and plasticity of modes of parity—that is, the idea that annual‐semelparous and perennial‐iteroparous life histories are better understood as endpoints along a continuum of possible strategies. I conclude that parity should be understood as a continuum of different modes of parity, which differ by the degree to which they disperse or concentrate reproductive effort in time. I further argue that there are three main implications of this conclusion: (1) that seasonality should not be conflated with parity; (2) that mathematical models purporting to explain the general evolution of semelparous life histories from iteroparous ones (or vice versa) should not assume that organisms can only display either an annual‐semelparous life history or a perennial‐iteroparous one; and (3) that evolutionary ecologists should base explanations of how different life‐history strategies evolve on the physiological or molecular basis of traits underlying different modes of parity.     

Temporal variation in reproductive costs and payoffs shapes the flowering strategy of a neotropical milkweed, <Emphasis Type="Italic">Asclepias curassavica</Emphasis>

A central goal of evolutionary ecology is to understand the factors that select for particular life history strategies, such as delaying reproduction. For example, environmental variation and reproductive costs to survival and growth often select for reproductive delays in semelparous and iteroparous species. In this study, we examine how variation in reproductive cost, which we define as a reduction to growth, survival, or future reproduction after a reproductive event, may select for reproductive delay in an iteroparous Neotropical milkweed with no obvious reproductive season. We analyzed demographic data collected every 3 months for 3 years from four populations of Asclepias curassavica in Monteverde, Costa Rica. We detected costs of flowering to survival and growth that varied in magnitude between our 12 transition periods without a seasonal pattern. The populations also exhibited temporal variation in reproductive payoffs measured as seedling establishment. We incorporated these reproductive costs into demographic projection models, which predicted a delayed flowering strategy only when we included temporal variation in costs and payoffs. Temporal variation in reproductive costs and payoffs is an important selective force in the evolution of delayed flowering in iteroparous species. Further, a lack of predictable seasonal pattern to reproductive costs and payoffs may contribute to the lack of seasonal reproductive patterns observed in our study species and other Neotropical species.     

A comparison of reproductive allocation and reproductive effort between semelparous and iteroparous fucoids (Fucales,Phaeophyta)

Reproductive allocation, the proportion of total dry weight allocated to receptacle tissue and reproductive effort, the proportion of reproductive carbon requirement contributed by receptacle photosynthesis, were measured in two fucoid algal species Fucus serratus and Himanthalia elongata at sites in NE Scotland. Reproductive development takes over ten months in H. elongata, a semelparous (single reproductive event) species, and reproductive allocation at receptacle maturity is over 98%. Following gamete release, the whole thallus dies. In contrast, reproductive development in F. serratus takes four months. Fucus serratus is iteroparous (capable of multiple reproductive events), reproductive allocation is 38.6% for the first reproductive event and 50.5% for the following year's event. In Fucus serratus, the receptacles appear to make a major contribution to their own carbon requirements after the first month of reproductive development. The receptacles of Himanthalia elongata contribute only a small proportion of the receptacle carbon requirements in the first four months of reproductive development, after which the contribution made through receptacle photosynthesis increases.     

Demographic diversity and sustainable fisheries

Fish species are diverse. For example, some exhibit early maturation while others delay maturation, some adopt semelparous reproductive strategies while others are iteroparous, and some are long-lived and others short-lived. The diversity is likely to have profound effects on fish population dynamics, which in turn has implications for fisheries management. In this study, a simple density-dependent stage-structured population model was used to investigate the effect of life history traits on sustainable yield, population resilience, and the coefficient of variation (CV) of the adult abundance. The study showed that semelparous fish can produce very high sustainable yields, near or above 50% of the carrying capacity, whereas long-lived iteroparous fish can produce very low sustainable yields, which are often much less than 10% of the carrying capacity. The difference is not because of different levels of sustainable fishing mortality rate, but because of difference in the sensitivity of the equilibrium abundance to fishing mortality. On the other hand, the resilience of fish stocks increases from delayed maturation to early maturation strategies but remains almost unchanged from semelparous to long-lived iteroparous. The CV of the adult abundance increases with increased fishing mortality, not because more individuals are recruited into the adult stage (as previous speculated), but because the mean abundance is more sensitive to fishing mortality than its standard deviation. The magnitudes of these effects vary depending on the life history strategies of the fish species involved. It is evident that any past high yield of long-lived iteroparous fish is a transient yield level, and future commercial fisheries should focus more on fish that are short-lived (including semelparous species) with high compensatory capacity.     

Reproductive effort,fecundity and energy allocation in two species of the genus Perinereis (Polychaeta: Nereididae)

Summary

The reproductive effort in terms of fecundity and energy allocation was studied in two species of semelparous polychaetes belonging to the genus Perinereis, living in the same environment, with different reproductive modalities. There is a great individual variability both in terms of reproductive effort and fecundity. Fecundity varied from 4080 to 15000 oocytes in P. rullieri and from 7000 to 26000 in P. cultrifera; no linear relationship was found between oocyte number and total jaw length utilised as size index. The energy content of germinal and somatic tissues was determined by Differential Scanning Calorimeter (DSC). The reproductive effort was calculated as RE = E_G/(E_G + E_S) where E_G is the total energy in germinal tissues and E_S is the total energy in somatic tissues. Reproductive effort is very high with mean values of 0.62 for P. rullieri and 0.79 for P. cultrifera. The different amounts of energy allocated in germinal tissues can be attributed to the different reproductive modalities—P. rullieri reproduces in the atokous phase whereas P. cultrifera has conserved epitoky in its life-cycle. The lack of correlation between reproductive effort and size index strongly suggests that reproductive allocation does not increase with age. In semelparous species the variability in fecundity and reproductive effort observed cannot be interpreted in terms of a trade-off between fecundity and survival as in iteroparous species. In fact, in semelparous an individual allocates all available resources to reproduction and then dies.     

Empirical evidence of a trade-off between reproductive effort and expectation of future reproduction in female three-spined sticklebacks

Optimal life-history models generally predict that the reproductive effort of iteroparous organisms may increase with age, as their expectation of future reproduction decreases. The population of three-spined sticklebacks (Gasterosteus aculeatus) in the Camargue (Rhone River Delta, France) is annual, all adults dying after their first breeding season. As the three-spined stickleback is a multiple spawner, we tested the hypothesis that reproductive effort may increase during the breeding season on field data. From 1987 to 1998, 653 female sticklebacks were collected in the field during the breeding seasons. The body size, body weight and weights of the liver, gonads and carcass were measured for these individuals. Only gravid females with mature eggs (176 fish) were included in the analysis. Considering the female three-spined stickleback as a capital breeder, the energetic resources available for allocation between soma and gonads were estimated by its body weight. Somatic condition decreased during the breeding season and reproductive effort (gonad weight relative to body weight) increased. These patterns did not vary significantly between years. These observed variations in reproductive effort during the breeding season can be interpreted as empirical evidence of a trade-off between reproductive effort and expectation of future reproduction.     

Reproductive effort,fecundity and energy allocation in Marphysa sanguinea (Polychaeta: Eunicidae)

Summary

Reproductive effort in terms of fecundity and energy allocation was studied in the iteroparous and long lived polychaete Marphysa sanguinea. Both measures show great variability. Fecundity varied from 8500 to 24300 oocytes; no linear relationship was found between oocyte number and jaw length whereas a direct relationship was established between oocyte number and wet body weight. The energy content of germinal and somatic tissues was determined by differential scanning calorimeter (DSC). The reproductive effort for a single reproductive event was calculated according to the formula: RE = E_G/(E_G + E_S) where E_Gis the total energy of the germinal tissues and E_S is the total energy of the somatic tissues. The lack of correlation between reproductive effort and size index strongly suggests that reproductive allocation does not increase with age. The reproductive effort ranged from 0.04 to 0.19 with a mean value of 0.120.     

Facultative semelparity in capelin Mallotus villosus (Osmeridae)-an experimental test of a life history phenomenon in a sub-arctic fish

Two alternative reproductive modes are present in fishes and reflect the age-specific mortality encountered through ontogenesis. Life-history hypotheses suggest that semelparity (i.e. death after a single reproductive event) evolves when the ratio of juvenile to adult survival is relatively high. Conversely, a relatively low ratio of juvenile to adult survival will favour iteroparity (i.e. death after two or more reproductive events). Fisheries management associates capelin (Mallotus villosus) spawning with mass mortality and semelparity even though life history models developed for this species suggest that females may follow an iteroparous trajectory. Capelin may spawn either inter-tidally on the beach or offshore in deeper, ocean waters but post-spawning survival and potential iteroparity has been notoriously difficult to assess in natural populations. Through a series of aquarium experiments we tested post-spawning survivability in a beach spawning and an ocean spawning population. The findings demonstrate that capelin which spawn offshore are absolute semelparous (death of both genders) while beach spawning capelin are iteroparous irrespective of sex. Beach spawning capelin regenerated ripe gonads from one spawning season to the next and provides the first conclusive evidence that capelin is physiologically capable of an iteroparous reproductive mode. The potential physical and biological processes which generate certain reproductive patterns in capelin are summarized and discussed in relation to life history hypotheses. We suggest that capelin is a facultative semelparous species in which dynamic changes within the semelparity-iteroparity continuum may occur as a result of subtle interactions between the spawning habitat, physical forcing, and predatory pressure.     

Of chickens and eggs: diverging propagule size of iteroparous and semelparous organisms

Interactive effects of two or more life-history traits on fitness have the potential to create suites of coadapted traits. Propagule (egg or seed) size is one such trait that is believed to have undergone coadaptation with other traits. Phylogenetic analyses of salmonid fishes have revealed an association between large eggs and semelparity, leading to the question of which came first. It has been hypothesized that an increased egg size would have increased juvenile relative to adult survival, favoring a subsequent increase in reproductive effort and eventually semelparity. Others have suggested that this is insufficient to cause a shift in parity, implying to the contrary that semelparity gave rise to larger eggs. In a previous study we showed that environmental unpredictability might select for production of larger propagules. Here we use simulations to directly model how propagule size evolves in response to environmental unpredictability with varying degrees of iteroparity. Our results demonstrate that environmental unpredictability causes pronounced propagule size divergence between iteroparous and purely semelparous species in taxa with a fixed age at maturity (e.g., pure annual species). However, even rare incidents of repeat breeding are sufficient to reduce selection for larger propagules substantially and thus divergence. Furthermore, introducing variation in age at maturity within propagule size genotypes has evolutionary effects similar to that of repeat breeding. Environmental unpredictability is thus unlikely to provide a general alternative explanation for the observed egg size divergence between iteroparous and semelparous salmonids.     

Comparative studies of epididymal morphology and sperm distribution in dasyurid marsupials during the breeding season

The structural features of the epididymis and the number and distribution of spermatozoa along the duct, during the breeding season, were examined in two semelparous and three iteroparous dasyurid marsupials. Total numbers of epididymal spermatozoa were extremely low in all of these species when compared with epididymal sperm numbers in most other marsupials and eutherian mammals. Although semelparous dasyurids had significantly more epididymal spermatozoa than itcroparous species, very few spermatozoa were seen in the distal cauda epididymidis of any of the species examined. This coincided with distinct changes in duct shape and the surface area of the lumen in caudal regions which resulted in a reduced sperm storage capacity in the cauda epididymidis of these species. The data suggest that, like Antechinus stuartii (Taggart & Temple-Smith, 1990a), sperm content of the ejaculates in these species will be extremely low, and that sperm motility and/or transport in the female tract is highly efficient. The functional and evolutionary significance of the reproductive strategies of semelparous and iteroparous dasyurid marsupials is still obscure and further study is needed to determine if the length of sperm storage in the female and sperm competition for storage sites is related to sperm distribution in the male and mating activities. This study does, however, clearly indicate that large numbers of spermatozoa are not required to ensure successful fertilization in either semelparous or iteroparous members of the family Dasyuridae.     

Terminal investment and senescence in rhesus macaques (Macaca mulatta) on Cayo Santiago

Long-lived iteroparous species often show aging-related changes in reproduction that may be explained by 2 non-mutually exclusive hypotheses. The terminal investment hypothesis predicts increased female reproductive effort toward the end of the life span, as individuals have little to gain by reserving effort for the future. The senescence hypothesis predicts decreased female reproductive output toward the end of the life span due to an age-related decline in body condition. Nonhuman primates are ideal organisms for testing these hypotheses, as they are long lived and produce altricial offspring heavily dependent on maternal investment. In this study, we integrated 50 years of continuous demographic records for the Cayo Santiago rhesus macaque (Macaca mulatta) population with new morphometric and behavioral data to test the senescence and terminal investment hypotheses. We examined relationships between maternal age and activity, mother and infant body condition, interbirth intervals, measures of behavioral investment in offspring, and offspring survival and fitness to test for age-associated declines in reproduction that would indicate senescence, and for age-associated increases in maternal effort that would indicate terminal investment. Compared with younger mothers, older mothers had lower body mass indices and were less active, had longer interbirth intervals, and spent more time in contact with infants, but had infants of lower masses and survival rates. Taken together, our results provide strong evidence for the occurrence of reproductive senescence in free-ranging female rhesus macaques but are also consistent with some of the predictions of the terminal investment hypothesis.     

Reproductive success and failure: the role of winter body mass in reproductive allocation in Norwegian moose

A life history strategy that favours somatic growth over reproduction is well known for long-lived iteroparous species, especially in unpredictable environments. Risk-sensitive female reproductive allocation can be achieved by a reduced reproductive effort at conception, or the subsequent adjustment of investment during gestation or lactation in response to unexpected environmental conditions or resource availability. We investigated the relative importance of reduced investment at conception compared with later in the reproductive cycle (i.e. prenatal, perinatal or neonatal mortality) in explaining reproductive failure in two high-density moose (Alces alces) populations in southern Norway. We followed 65 multiparous, global positioning system (GPS)-collared females throughout the reproductive cycle and focused on the role of maternal nutrition during gestation in determining reproductive success using a quasi-experimental approach to manipulate winter forage availability. Pregnancy rates in early winter were normal (≥0.8) in all years while spring calving rates ranged from 0.4 to 0.83, with prenatal mortality accounting for most of the difference. Further losses over summer reduced autumn recruitment rates to 0.23–0.69, despite negligible predation. Over-winter mass loss explained variation in both spring calving and autumn recruitment success better than absolute body mass in early or late winter. Although pregnancy was related to body mass in early winter, overall reproductive success was unrelated to pre-winter body condition. We therefore concluded that reproductive success was limited by winter nutritional conditions. However, we could not determine whether the observed reproductive allocation adjustment was a bet-hedging strategy to maximise reproduction without compromising survival or whether females were simply unable to invest more resources in their offspring.     

Evolution of delayed reproduction in uncertain environments: a life-history perspective

Environmental uncertainty alone can select for delayed reproduction; however, its relative role in the evolution of delayed reproduction across life histories is not known. Along a life-history spectrum from low-survival/high-fertility species to high-survival/low-fertility species, we show that the latter are more likely to evolve delayed reproduction if fertility varies over time. By contrast, if survival varies over time, low-survival life histories are more likely to evolve delays. If there is variation in both survival and fertility, and if this variation is positively associated, the evolutionarily stable reproductive delay is decreased (relative to independent variation in survival and fertility). Conversely, if variation in survival and fertility is negatively associated, the evolutionarily stable reproductive delay is increased. We further show that environmental uncertainty can drive the evolution of delayed reproduction in an iteroparous organism but only in the special case where juvenile survival is greater than adult survival. For common iteroparous life histories (adult survival > juvenile survival), environmental uncertainty does not select for delayed reproduction. Thus, any benefits that delayed reproduction might have on reproduction or survival could be especially important in explaining the common observation of delayed reproduction in many vertebrates and perennial plants.