A review of the reproductive bionomics of aquatic gammaridean amphipods: variation of life history traits with latitude,depth, salinity and superfamily

Life history traits (mean and maximum body length of females, number of embryos per brood = brood size, embryo diameter, number of broods per female, lifespan of females) for 302 populations of aquatic gammaridean amphipods, representing 214 species in 16 superfamilies, were reviewed. The variation of these traits, of lifetime potential fecundity (i.e. the number of embryos produced per female lifespan) and of reproductive potential (i.e. the number of embryos produced per female per year), with temperature (latitude), depth, salinity and superfamily, was investigated by various univariate and multivariate methods. Gammaridean amphipods comprise semelparous and iteroparous populations and species, with semiannual, annual, biannual or perennial life cycles. However, most gammarideans studied so far are iteroparous annuals. Body length explains most of the variation in brood size and embryo diameter. The reproductive potential may be increased by increasing body size for a constant breeding frequency, by increasing brood size at the expense of smaller embryos, by increasing breeding frequency for a constant lifespan at the expense of smaller individual broods and/or embryos, and by increasing longevity for a constant breeding frequency and brood size. Combinations of these different options constitute the life history patterns of gammarideans, which vary across superfamilies, latitude and depth, and cannot simply be explained by variations in body length. High latitude species were generally characterized by biannual or perennial life histories, large body size, delayed maturity, and single or few broods with many, relatively large embryos; converse sets of traits characterized low latitude species. Deep-living species had relatively smaller broods and embryos than their shallow-living relatives, yet did not produce more broods. However, different superfamilies dominated in different habitats. The importance of natural selection relative to phylogenetic (historical) and physiological constraints in the forging of these patterns is discussed.     

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.     

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).     

Sperm production, storage, and the synchronization of male and female reproductive cycles in the iteroparous, stripe-faced dunnart (Sminthopsis macroura; Marsupialia): relationship to reproductive strategies within the Dasyuridae

Seasonal changes in the number and distribution of spermatozoa in males, and annual changes in the distribution of litters and embryos in females were examined in the iteroparous dasyurid marsupial, Sminthopsis macroura , in captivity. Total number of sperm in the testis (0.53 × 10⁶ sperm/testis) and epididymidis (0.54 × 10⁶ sperm/epididymidis) were extremely low when compared with those in other marsupials and eutherian mammals. Testicular sperm production and epididymal sperm reserves were high between May and October and declined to a minimum in March. These changes reflected monthly changes in testicular and epididymal weight and testis morphology. Data on changing epididymal sperm distribution suggest that sperm storage in the cauda epididymidis is limited and that few sperm are required for successful insemination. Litters were born between June and January, with most litters occurring between July and October. Second pregnancies occurred between October and January, with a peak in December. The data indicate that the timing of mating activity and litter production by S. macroura correspond very closely with the period of maximum sperm production by males. The synchrony of these events contrasts dramatically with that of similar-sized semelparous dasyurid species. It is hypothesized that testicular failure prior to the mating season, copulatory behaviour, and possibly male die-off in dasyurid marsupials are related to the degree of competition between males for mates and, hence, population density and environmental predictability. These data suggest that intermale sperm competition is affected by the periods of female receptivity and the length of sperm storage in the female reproductive tract. Fundamental differences in the reproductive strategies of iteroparous and semelparous dasyurid marsupials are discussed.     

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.     

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.     

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.

     

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.     

Ontogenetic patterns and phylogenetic trends in freshwater flatworms (Tricladida); constraint or selection?

Semelparity and iteroparity are unevenly distributed among the families of the Paludicola and this implies that there have been taxonomic restrictions on life-history evolution. Species differ in their investments in reproduction and high levels can be related, causally, to reduced life-spans; i.e. semelparous species invest more in reproduction than iteroparous species. However, there does not appear to be any fundamental reason why the extent and timing of these investments should not be open to modification by natural selection.A major morphological difference between the predominantly semelparous Dendrocoelidae and the predominantly iteroparous Dugesiidae and Planariidae is the presence of an anterior adhesive organ; dendrocoelids have one, but members of the other families do not. A plausible scenario can be formulated relating this structure, causally, to enhanced juvenile survivorship which, in turn, favors the semelparous life history.     

Development and phenotypic variability of genetically identical half mouse embryos

The growth and development of three groups of genetically identical F1 C57BL/6J female x SJL/J male mice were compared to examine whether embryo manipulation affects subsequent postnatal growth and development of mammalian embryos: (1) controls--the natural offspring of timed matings, (2) transferred controls--offspring from 2-cell embryos transferred to recipients 1 day asynchronous, and (3) transferred half embryos--offspring developing from one blastomere from the 2-cell stage transferred to recipients 1 day asynchronous. The recipients were C57BL/6J females. No differences were found in the age at eye opening and vaginal opening. At 5 days after birth the median body weights of the controls were lower than the weights of the transferred groups. This result could be explained by the larger litter size in the control group. The overall variances of the body weights did not differ between the groups. By the second week after birth a marked increase in overall variances of body weights of the transferred groups, compared with the control group, was observed. At 5 days after birth, the median tail lengths did not differ between groups, and overall variances were the same. By the second week, the overall variances of the tail lengths of the transferred groups were significantly greater than that of the control group. Possibly the increased overall variances of the body weight and the tail length of the transferred groups are related to the smaller litter size in these groups which affects competition for food and the ambient temperature in the nest. The overall results suggest newborn mice that have developed from half embryos have compensated for their initial deficiency. The intraclass correlation coefficients for body weight and tail length are approximately the same in all groups. Thus, producing artificial identical twins by embryo bisection may not affect their potential usefulness in the design of experiments.     

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.     

COEVOLUTIONARY FEEDBACKS BETWEEN FAMILY INTERACTIONS AND LIFE HISTORY

Families with parental care show a parent–offspring conflict over the amount of parental investment. To date, the resolution of this conflict was modeled as being driven by either purely within‐brood or between‐brood competition. In reality the partitioning of parental resources within‐ versus between‐broods is an evolving life history trait, which can be affected by parent–offspring interactions. This coevolutionary feedback between life history and family interactions may influence the evolutionary process and outcome of parent–offspring coadaptation. We used a genetic framework for a simulation model where we allowed parental parity to coevolve with traits that determine parental investment. The model included unlinked loci for clutch size, parental sensitivity, baseline provisioning, and offspring begging. The simulation showed that tight coadaptation of parent and offspring traits only occurred in iteroparous outcomes whereas semelparous outcomes were characterized by weak coadaptation. When genetic variation in clutch size was unrestricted in the ancestral population, semelparity and maximal begging with poor coadaptation evolved throughout. Conversely, when genetic variation was limited to iteroparous conditions, and/or when parental sensitivity was treated as an evolutionarily fixed sensory bias, coadapted outcomes were more likely. Our findings show the influence of a feedback between parity, coadaptation, and conflict on the evolution of parent–offspring interactions.     

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.     

Costs of reproduction and terminal investment by females in a semelparous marsupial

Evolutionary explanations for life history diversity are based on the idea of costs of reproduction, particularly on the concept of a trade-off between age-specific reproduction and parental survival, and between expenditure on current and future offspring. Such trade-offs are often difficult to detect in population studies of wild mammals. Terminal investment theory predicts that reproductive effort by older parents should increase, because individual offspring become more valuable to parents as the conflict between current versus potential future offspring declines with age. In order to demonstrate this phenomenon in females, there must be an increase in maternal expenditure on offspring with age, imposing a fitness cost on the mother. Clear evidence of both the expenditure and fitness cost components has rarely been found. In this study, we quantify costs of reproduction throughout the lifespan of female antechinuses. Antechinuses are nocturnal, insectivorous, forest-dwelling small (20-40 g) marsupials, which nest in tree hollows. They have a single synchronized mating season of around three weeks, which occurs on predictable dates each year in a population. Females produce only one litter per year. Unlike almost all other mammals, all males, and in the smaller species, most females are semelparous. We show that increased allocation to current reproduction reduces maternal survival, and that offspring growth and survival in the first breeding season is traded-off with performance of the second litter in iteroparous females. In iteroparous females, increased allocation to second litters is associated with severe weight loss in late lactation and post-lactation death of mothers, but increased offspring growth in late lactation and survival to weaning. These findings are consistent with terminal investment. Iteroparity did not increase lifetime reproductive success, indicating that terminal investment in the first breeding season at the expense of maternal survival (i.e. semelparity) is likely to be advantageous for females.     

Population structure and growth of the Japanese littleneck clam <Emphasis Type="Italic">Ruditapes philippinarum</Emphasis> in Amursky Bay,Sea of Japan

This paper deals with the size, age, and sex structure of population and growth of the Japanese littleneck clam Ruditapes philippinarum in Amursky Bay (Peter the Great Bay, Sea of Japan). One-year-olds and individuals with a shell length less than 19.8 mm were not found in the population under study. The population consisted mostly of 3-4-year-old clams (72.4%) with a shell length of 35–45 mm (67.8%). The maximum recorded age of R. philippinarum was 7 years, and maximum shell length was 52.7 mm. The male to female ratio was approximately 2: 1. Hermaphroditism (2.1%) and parasitic castration (1.4%) were observed. Linear growth rates of clams were found to increase until the age of three years old (11.6 ± 0.6 mm/year). Mollusks reach a commercial size of over 35 mm in shell length in the fourth year of life. The parameters of the von Bertalanffy equation describing group linear growth were L _∞ = 56.6 mm, k = 0.302 year^?1, and t ₀ = 0.468 year. The relationship between the shell length and the wet body weight is described by the equation W = 0.000253L^2.954.     

The Impact of Maternal Uterine Genotype on Postnatal Growth and Adult Body Size in Mice

Embryo transfers were used to demonstrate that the genotype of the mother providing the uterine developmental environment significantly influences postnatal growth and adult body size of her progeny. Irrespective of their own genotype, mouse embryos transferred into the uterus of an inbred strain with large body size (C3H) had greater body weights, longer tails and higher growth rates than those transferred into the uterus of a strain with small body size (SWR). Uterine heterosis on body size was smaller than progeny heterosis, and both progeny and uterine heterosis persisted in adult mice. Uterine litter size was significantly negatively associated with body weight, tail length, growth rate and the timing of developmental events. The inbred SWR strain was more sensitive to the embryo transfer procedure than the C3H strain, but effects due to embryo transfer were moderate. Prenatal uterine effects have ramifications for biotechnologies utilizing embryo transfer as well as predictions about evolutionary change by selection.     

Early onset of reproductive senescence in domestic sheep Ovis aries

A central theme in life history theory is to determine how reproduction varies with age in iteroparous organisms. Evidence of ageing and senescence, defined as the progressive loss of function accompanied by decreased performance with age, remains poorly documented for large herbivores, in particular as it relates to reproduction. Analyses of body weight of 87 532 domestic sheep lambs demonstrates that onset of reproductive senescence in ewes occurs already at 5 and 6 years of age when measured, respectively, as lamb weight and litter size produced. This provides convincing evidence of early onset of reproductive senescence in this highly domesticated sheep breed. As this is earlier than indicated for other Ovis species as well as for the Soay sheep, an ancient and lightly domesticated sheep, we hypothesize that there may be a cost of selection for large litter size in mammalian herbivores.     

Deciphering the complex nature of bolting time regulation in <Emphasis Type="Italic">Beta vulgaris</Emphasis>

Key message

Only few genetic loci are sufficient to increase the variation of bolting time in Beta vulgaris dramatically, regarding vernalization requirement, seasonal bolting time and reproduction type.

Abstract

Beta species show a wide variation of bolting time regarding the year of first reproduction, seasonal bolting time and the number of reproduction cycles. To elucidate the genetics of bolting time control, we used three F₃ mapping populations that were produced by crossing a semelparous, annual sugar beet with iteroparous, vernalization-requiring wild beet genotypes. The semelparous plants died after reproduction, whereas iteroparous plants reproduced at least twice. All populations segregated for vernalization requirement, seasonal bolting time and the number of reproduction cycles. We found that vernalization requirement co-segregated with the bolting locus B on chromosome 2 and was inherited independently from semel- or iteroparous reproduction. Furthermore, we found that seasonal bolting time is a highly heritable trait (h ² > 0.84), which is primarily controlled by two major QTL located on chromosome 4 and 9. Late bolting alleles of both loci act in a partially recessive manner and were identified in both iteroparous pollinators. We observed an additive interaction of both loci for bolting delay. The QTL region on chromosome 4 encompasses the floral promoter gene BvFT2, whereas the QTL on chromosome 9 co-localizes with the BR ₁ locus, which controls post-winter bolting resistance. Our findings are applicable for marker-assisted sugar beet breeding regarding early bolting to accelerate generation cycles and late bolting to develop bolting-resistant spring and winter beets. Unexpectedly, one population segregated also for dwarf growth that was found to be controlled by a single locus on chromosome 9.

     

Target size and optimal life history when individual growth and energy budget are stochastic

I extend my previous work on life history optimization when body mass is divided into reserves and structure components. Two important innovations are: (1) effect of finite target size on optimal structural growth; (2) incorporating reproduction in the optimization objective. I derive optimal growth trajectories and life histories, given that the individual is subject to both starvation mortality and exogenous hazards (e.g., predation). Because of overhead costs in building structural mass, it is optimal to stop structural growth close to the target size, and to proceed only by accumulating reserves. Higher overhead costs cause earlier cessation of structural growth and smaller final structures. Semelparous reproduction also promotes early cessation of structural growth, compared to when only survival to target size is maximized. In contrast, iteroparous reproduction can prolong structural growth, resulting in larger final structures than in either the survival or the semelparous scenarios. Increasing the noise in individual growth lowers final structural mass at small target sizes, but the effect is reversed for large target sizes. My results provide predictions for comparative studies. I outline important consequences of my results to additional important evolutionary questions: evolution of sexual dimorphism, optimization of clutch size and evolution of progeny and adult sizes.     

Beyond lifetime reproductive success: the posthumous reproductive dynamics of male Trinidadian guppies

In semelparous populations, dormant germ banks (e.g. seeds) have been proposed as important in maintaining genotypes that are adaptive at different times in fluctuating environments. Such hidden storage of genetic diversity need not be exclusive to dormant banks. Genotype diversity may be preserved in many iteroparous animals through sperm-storage mechanisms in females. This allows males to reproduce posthumously and increase the effective sizes of seemingly female-biased populations. Although long-term sperm storage has been demonstrated in many organisms, the understanding of its importance in the wild is very poor. We here show the prevalence of male posthumous reproduction in wild Trinidadian guppies, through the combination of mark–recapture and pedigree analyses of a multigenerational individual-based dataset. A significant proportion of the reproductive population consisted of dead males, who could conceive up to 10 months after death (the maximum allowed by the length of the dataset), which is more than twice the estimated generation time. Demographic analysis shows that the fecundity of dead males can play an important role in population growth and selection.