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.     

Reproductive efficiency and shade avoidance plasticity under simulated competition

Plant strategy and life‐history theories make different predictions about reproductive efficiency under competition. While strategy theory suggests under intense competition iteroparous perennial plants delay reproduction and semelparous annuals reproduce quickly, life‐history theory predicts both annual and perennial plants increase resource allocation to reproduction under intense competition. We tested (1) how simulated competition influences reproductive efficiency and competitive ability (CA) of different plant life histories and growth forms; (2) whether life history or growth form is associated with CA; (3) whether shade avoidance plasticity is connected to reproductive efficiency under simulated competition. We examined plastic responses of 11 herbaceous species representing different life histories and growth forms to simulated competition (spectral shade). We found that both annual and perennial plants invested more to reproduction under simulated competition in accordance with life‐history theory predictions. There was no significant difference between competitive abilities of different life histories, but across growth forms, erect species expressed greater CA (in terms of leaf number) than other growth forms. We also found that shade avoidance plasticity can increase the reproductive efficiency by capitalizing on the early life resource acquisition and conversion of these resources into reproduction. Therefore, we suggest that a reassessment of the interpretation of shade avoidance plasticity is necessary by revealing its role in reproduction, not only in competition of plants.     

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.     

Testing the effect of early‐life reproductive effort on age‐related decline in a wild insect

The disposable soma theory of ageing predicts that when organisms invest in reproduction they do so by reducing their investment in body maintenance, inducing a trade‐off between reproduction and survival. Experiments on invertebrates in the lab provide support for the theory by demonstrating the predicted responses to manipulation of reproductive effort or lifespan. However, experimental studies in birds and evidence from observational (nonmanipulative) studies in nature do not consistently reveal trade‐offs. Most species studied previously in the wild are mammals and birds that reproduce over multiple discrete seasons. This contrasts with temperate invertebrates, which typically have annual generations and reproduce over a single season. We expand the taxonomic range of senescence study systems to include life histories typical of most temperate invertebrates. We monitored reproductive effort, ageing, and survival in a natural field cricket population over ten years to test the prediction that individuals investing more in early‐reproduction senesce faster and die younger. We found no evidence of a trade‐off between early‐life reproductive effort and survival, and only weak evidence for a trade‐off with phenotypic senescence. We discuss the possibility that organisms with multiple discrete breeding seasons may have greater opportunities to express trade‐offs between reproduction and senescence.     

Stress promotes changes in resource allocation to growth and reproduction in a simultaneous hermaphrodite with indeterminate growth

In iteroparous animals, investment in growth is compromised by investment in reproduction, especially in species with indeterminate growth. Life‐history theory predicts that growth should be favoured over reproduction, assuming size‐related fecundity or survival. Hence, increase body condition represents an increase in reproductive potential. Simultaneous hermaphrodites should adjust their resource allocation to each sex function in response to current conditions but, recently, it has been suggested that, in hermaphrodites, gender allocation should be considered as a three‐way trade‐off, including the investment in somatic growth. Due to the higher costs involved, the female function is affected to a greater extent by environmentally stressful conditions rather than the male function. To examine this, we induced stress in the hermaphroditic earthworm Eisenia fetida (Savigny, 1826) and looked for changes in resource allocation in nonreproductive and reproductive individuals. Experimental stress was induced by using tweezers to elicit contractile escape movements. We predicted that stressed earthworms would preferentially allocate resources to growth. In nonreproductive individuals, however, stress had a negative effect on growth, although weight recovery was rapid once manipulation ceased, indicating the importance of body condition, as well as the existence of mechanisms of compensatory growth for growth trajectories in this earthworm species. The response of reproductive individuals was consistent with our expectation: (1) stressed worms maintained their growth rate at the expense of current reproduction and (2) stressed earthworms laid 25% fewer cocoons, which were 30% lighter than cocoons laid by control earthworms. The present results suggest that E. fetida regulates its reproductive effort and that future reproduction has more impact on its fitness than current reproduction. The trade‐off between current and future reproduction should be taken into consideration in models of sex allocation in simultaneous hermaphrodites. © 2007 The Linnean Society of London, Biological Journal of the Linnean Society, 2007, 91 , 593–600.     

Are certain life histories particularly prone to local extinction?

Using stochastic simulations and elasticity analysis, we show that there are inherent differences in the risk of extinction between life histories with different demographies. Which life history is the most vulnerable depends on which vital rate varies. When juvenile survival varies semelparous organisms with delayed reproduction are the most vulnerable ones, while a varying developmental rate puts a greater threat to semelparous organisms with rapid development. Iteroparous organisms are the most vulnerable ones when adult survival varies. Generally, we do not expect to observe organisms in nature having variation in vital rates that produce a high risk of extinction. Given the results here we therefore predict that iteroparous organisms should show low variation in adult survival. Moreover, we predict that semelparous organisms should show low variation in juvenile survival and low variation in developmental rate. The effect of temporal correlation on extinction risk is most pronounced in organisms with semelparous life histories.     

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.     

Reproductive effort in molluscs

Summary A survey of the available molluscan literature shows that reproductive effort is higher in semelparous species (29.90%) than in iteroparous species (18.21%), and that in iteroparous species reproductive effort increases with successive breeding seasons. Oviparous species were found to divert considerably more into reproduction than viviparous species, with 24.24% and 5.25% channeled respectively.     

Tradeoff between offspring mass and subsequent reproduction in a highly iteroparous mammal

When resources are limited, current maternal investment should reduce subsequent reproductive success or survival. We used longitudinal data on marked mountain goats Oreamnos americanus to assess if offspring mass at weaning affected maternal survival and future reproduction. Offspring mass was positively correlated with survival of old mothers, suggesting that mothers produced lighter kids, and hence reduced reproductive effort, in their last reproduction. Offspring mass at weaning did not affect survival of young and prime‐aged mothers, but females that had weaned heavy offspring had a reduced probability of subsequent reproduction in years of low population density. Because offspring survival is correlated with weaning mass, mothers’ allocation to reproduction involves a tradeoff between current and future fitness returns. We demonstrate for the first time that allocation to current offspring mass in an iteroparous mammal reduces the probability of subsequent reproduction.     

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.     

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.     

Herbivores and the evolution of the semelparous perennial life-history of plants

The relationship between a plant and its potential enemies changes drastically after reproduction has started. Using a dynamic modelling approach we study the effects of herbivores and pathogens, that are attracted by reproducing plants, on optimal allocation of resources, and life-history strategies. We assume that the level of attack increases with the investment in reproduction, which may lead to a reduction of current years reproductive success, a reduction of storage efficiency or an increase of plant mortality. If herbivores or pathogens attracted by flowering plants mainly reduce current years reproductive success, the optimal life-history is annual or iteroparous perennial if the attack is an all or nothing event. If the level of consumption increases with the number of herbivores attracted, the optimal life-history is most likely iteroparity with or without mast years. Only under very restricted conditions this may lead to semelparity. If herbivores mainly reduce the efficiency of the resources stored for next year, the optimal life-history is iteroparity. If herbivores mainly reduce survival, the optimal solution is likely to be mast years or semelparity. For parameter values that are realistic for Cynoglossum officinale, a semelparous perennial from calcereous soils, the model predicts that reproduction should start in the third year and that 99% of the available resources at the end of season should be invested in reproduction and only 1% saved for growth next year. With such an investment only c. 1% of the plants would survive after reproduction, so the optimal life-history is close to semelparity. For the small fraction of plants that reproduce more than once, years of vegetative growth only and years with reproduction should alternate. Multiple reproduction is rare in C. officinale. However, such a life history is very common for plants known as semelparous perennial. Although the available empirical evidence is, as yet, circumstantial rather than conclus ive we propose that reproduction related mortality mediated through herbivores or pathogens may play a role in the evolution of the semelparous perennial life-history.     

Interactions of environmental temperature with photoperiod in determining age at maturity in a semelparous polychaete Nereis (neanthes) virens sars

1. 1. Larger members of the Polychacta exhibit two contrasting life cycles: semelparous in the Nereidae, iteroparous in most others.

2. 2. In semelparous forms environmental interaction determines age at reproduction and fecundity in the single spawning event whereas in iteroparous forms such interaction influences the variable age specific reproductive effort.

3. 3. Development of aquaculture has created conditions where organisms are grown under conditions of optimum temperature for growth and unlimited food.

4. 4. We present data on the life history responses (reaction norms) of the semelparous Nereis virens in which age at death in natural populations varies between 3 to 8+ years.

5. 5. In Nereis virens minimum life span (= generation time) in culture is one year but the lifespan remains modular 12 months without manipulation of photoperiod.

6. 6. Environmental temperature plays two roles: i) in conjunction with energy availability to determine “age at first/only reproduction” and secondly as an element (with photoperiod) in the control of gametogenic processes imposing seasonality on the life cycle.

7. 7. The observations suggest that long generation time in natural populations of N. virens is associated with reduced growth rate and that low growth rate is associated with reproduction at a larger size.

     

Female reproduction bears no survival cost in captivity for gray mouse lemurs

The survival cost of reproduction has been revealed in many free‐ranging vertebrates. However, recent studies on captive populations failed to detect this cost. Theoretically, this lack of survival/reproduction trade‐off is expected when resources are not limiting, but these studies may have failed to detect the cost, as they may not have fully accounted for potential confounding effects, in particular interindividual heterogeneity. Here, we investigated the effects of current and past reproductive effort on later survival in captive females of a small primate, the gray mouse lemur. Survival analyses showed no cost of reproduction in females; and the pattern was even in the opposite direction: the higher the reproductive effort, the higher the chances of survival until the next reproductive event. These conclusions hold even while accounting for interindividual heterogeneity. In agreement with aforementioned studies on captive vertebrates, these results remind us that reproduction is expected to be traded against body maintenance and the survival prospect only when resources are so limiting that they induce an allocation trade‐off. Thus, the cost of reproduction has a major extrinsic component driven by environmental conditions.     

Costs of reproduction can explain the correlated evolution of semelparity and egg size: theory and a test with salmon

Species’ life history traits, including maturation age, number of reproductive bouts, offspring size and number, reflect adaptations to diverse biotic and abiotic selection pressures. A striking example of divergent life histories is the evolution of either iteroparity (breeding multiple times) or semelparity (breed once and die). We analysed published data on salmonid fishes and found that semelparous species produce larger eggs, that egg size and number increase with salmonid body size among populations and species and that migratory behaviour and parity interact. We developed three hypotheses that might explain the patterns in our data and evaluated them in a stage‐structured modelling framework accounting for different growth and survival scenarios. Our models predict the observation of small eggs in iteroparous species when egg size is costly to maternal survival or egg number is constrained. By exploring trait co‐variation in salmonids, we generate new hypotheses for the evolution of trade‐offs among life history traits.     

Density-dependent vital rates and their population dynamic consequences

We explore a set of simple, nonlinear, two-stage models that allow us to compare the effects of density dependence on population dynamics among different kinds of life cycles. We characterize the behavior of these models in terms of their equilibria, bifurcations, and nonlinear dynamics, for a wide range of parameters. Our analyses lead to several generalizations about the effects of life history and density dependence on population dynamics. Among these are: (1) iteroparous life histories are more likely to be stable than semelparous life histories; (2) an increase in juvenile survivorship tends to be stabilizing; (3) density-dependent adult survival cannot control population growth when reproductive output is high; (4) density-dependent reproduction is more likely to cause chaotic dynamics than density dependence in other vital rates; and (5) changes in development rate have only small effects on bifurcation patterns. Received: 12 April 1999 / Published online: 3 August 2000     

Age at mating and male quality influence female patterns of reproductive investment and survival

The trade‐off between the allocation of resources toward somatic maintenance or reproduction is one of the fundamentals of life history theory and predicts that females invest in offspring at the expense of their longevity or vice versa. Mate quality may also affect life history trade‐offs through mechanisms of sexual conflict; however, few studies have examined the interaction between mate quality and age at first mating in reproductive decisions. Using house crickets (Acheta domesticus), this study examines how survival and reproductive trade‐offs change based on females’ age at first reproduction and exposure to males of varying size. Females were exposed to either a large (presumably high‐quality) or small male at an early (young), middle (intermediate), or advanced (old) age, and longevity and reproductive investment were subsequently tracked. Females mated at a young age had the largest number of eggs but the shortest total lifespans while females mated at older ages produced fewer eggs but had longer total lifespans. The trade‐off between age at first mating and eggs laid appears to be mediated through higher egg‐laying rates and shorter postmating lifespans in females mated later in life. Exposure to small males resulted in shorter lifespans and higher egg‐laying rates for all females indicating that male manipulation of females, presumably through spermatophore contents, varies with male size in this species. Together, these data strongly support a trade‐off between age at first reproduction and lifespan and support the role of sexual conflict in shaping patterns of reproduction.     

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.     

DOES EVOLUTION OF ITEROPAROUS AND SEMELPAROUS REPRODUCTION CALL FOR SPATIALLY STRUCTURED SYSTEMS?

Abstract.— A persistent question in the evolution of life histories is the fitness trade-off between reproducing only once (semelparity) in a lifetime or reproducing repeated times in different seasons (iteroparity). The problem can be formulated into a research agenda by assuming that one reproductive strategy is resident (has already evolved) and by asking whether invasion (evolution) of an alternative reproductive strategy is possible. For a spatially nonstructured system, Bulmer (1994) derived the relationship v + PA < 1 (PA is adult survival; vbs and bs are offspring numbers for iteroparous and semelparous breeding strategies, respectively) at which semelparous population cannot be invaded by an iteroparous mutant. When the inequality is changed to v + PA > 1, invasion of a semelparous mutant is not possible. From the inequalities, it is easy to see that possibilities for evolutionary establishment of a novel reproductive strategy are rather narrow. We extended the evolutionary scenario into a spatially structured system with dispersal linkage among the subunits. In this domain, a rare reproductive strategy can easily invade a population dominated by a resident reproductive strategy. The parameter space enabling invasion is far more generous with spatially structured evolutionary scenarios than in a spatially nonstructured system.     

Herbivore-mediated ecological costs of reproduction shape the life history of an iteroparous plant

Plant reproduction yields immediate fitness benefits but can be costly in terms of survival, growth, and future fecundity. Life-history theory posits that reproductive strategies are shaped by trade-offs between current and future fitness that result from these direct costs of reproduction. Plant reproduction may also incur indirect ecological costs if it increases susceptibility to herbivores. Yet ecological costs of reproduction have received little empirical attention and remain poorly integrated into life-history theory. Here, we provide evidence for herbivore-mediated ecological costs of reproduction, and we develop theory to examine how these costs influence plant life-history strategies. Field experiments with an iteroparous cactus (Opuntia imbricata) indicated that greater reproductive effort (proportion of meristems allocated to reproduction) led to greater attack by a cactus-feeding insect (Narnia pallidicornis) and that damage by this herbivore reduced reproductive success. A dynamic programming model predicted strongly divergent optimal reproductive strategies when ecological costs were included, compared with when these costs were ignored. Meristem allocation by cacti in the field matched the optimal strategy expected under ecological costs of reproduction. The results indicate that plant reproductive allocation can strongly influence the intensity of interactions with herbivores and that associated ecological costs can play an important selective role in the evolution of plant life histories.