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).     

Comparative phylogenetic analysis of the evolution of semelparity and life history in salmonid fishes

The selective pressures involved in the evolution of semelparity and its associated life-history traits are largely unknown. We used species-level analyses, independent contrasts, and reconstruction of ancestral states to study the evolution of body length, fecundity, egg weight, gonadosomatic index, and parity (semelparity vs. degree of iteroparity) in females of 12 species of salmonid fishes. According to both species-level analysis and independent contrasts analysis, body length was positively correlated with fecundity, egg weight, and gonadosomatic index, and semelparous species exhibited a significantly steeper slope for the regression of egg weight on body length than did iteroparous species. Percent repeat breeding (degree of iteroparity) was negatively correlated with gonadosomatic index using independent contrasts analysis. Semelparous species had significantly larger eggs by species-level analysis, and the egg weight contrast for the branch on which semelparity was inferred to have originated was significantly larger than the other egg weight contrasts, corresponding to a remarkable increase in egg weight. Reconstruction of ancestral states showed that egg weight and body length apparently increased with the origin of semelparity, but fecundity and gonadosomatic index remained more or less constant or decreased. Thus, the strong evolutionary linkages between body size, fecundity, and gonadosomatic index were broken during the transition from iteroparity to semelparity. These findings suggest that long-distance migrations, which increase adult mortality between breeding episodes, may have been necessary for the origin of semelparity in Pacific salmon, but that increased egg weight, leading to increased juvenile survivorship, was crucial in driving the transition. Our analyses support the life-history hypotheses that a lower degree of repeat breeding is linked to higher reproductive investment per breeding episode, and that semelparity evolves under a combination of relatively high juvenile survivorship and relatively low adult survivorship.     

Environmental variability and semelparity vs. iteroparity as life histories

Research on the evolution of life histories addresses the topic of fitness trade-offs between semelparity (reproducing once in a lifetime) and iteroparity (repeated reproductive bouts per lifetime). Bulmer (1994) derived the relationship v+P(A)<1 (P(A) is the adult survival;vb(S) and b(S) are the offspring numbers for iteroparous and semelparous breeding strategies, respectively), under which a resident semelparous population cannot be invaded by an iteroparous mutant when the underlying population dynamics are stable. We took Bulmer's population dynamics, and added noise in juvenile and adult survival and in offspring numbers. Long-term coexistence of the two strategies is possible in much of the parameter region ofv +P(A)<1 when noise occurs simultaneously in all three components, or (more restricted) when it affects juvenile and adult survival or adult survival and offspring numbers. Iteroparity cannot persist when the environmental variability involves juvenile survival and offspring numbers, or when the noise acts on the three components separately.     

Stochasticity and spatial coexistence of semelparity and iteroparity as life histories

We investigate conditions enabling long-term coexistence of semelparity (reproducing only once per lifetime) and iteroparity (repeated spells of reproduction in subsequent breeding seasons). Bulmer (1985, 1994) has transferred the study of the fitness merit of reproducing semelparously vs. iteroparously into a density-dependent system, using an invasion scenario with an abundant resident population of one reproductive strategy and a rare mutant invader population of another reproductive strategy. For stable population dynamics, Bulmer (1994) derived condition v + P _A < 1 (P _A is adult survival and v is the ratio of offspring number of the iteroparous type over that of the semelparous type) where a semelparous population cannot be invaded by an iteroparous strategy. In order to study the generalisation of Bulmer's results in spatial population dynamics, we generate a population system consisting of a linear string of habitable sub-units. The sub-units are semi-independent, obeying discrete-time Ricker dynamics in renewal, but they are close enough for dispersing individuals to couple them together. At each time step, a random fraction of individuals in each sub-unit disperses into neighbourhood. In this setting, we observe long-term persistence of semelparity and iteroparity when dispersal is stochastic and positively autocorrelated. Stochasticity in dispersal creates fluctuating local dynamics and thus permits long-term persisting coexistence of semelparity and iteroparity even in the parameter region where Ricker dynamics are stable and the Bulmer inequality is true. Positively autocorrelated, in contrast to negatively autocorrelated dispersal time-series, promoted coexistence between semelparity and iteroparity.     

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.     

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.     

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.     

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.     

One clutch or two clutches? Fitness correlates of coexisting alternative female life-histories in the European earwig

Whether to reproduce once or multiple times (semelparity vs. iteroparity) is a major life-history decision that organisms have to take. Mode of parity is usually considered a species characteristic. However, recent models suggested that population properties or condition-dependent fitness payoffs could help to maintain both life-history tactics within populations. In arthropods, semelparity was also hypothesised to be a critical pre-adaptation for the evolution of maternal care, semelparous females being predicted to provide more care due to the absence of costs on future reproduction. The aim of this study was to characterize potential fitness payoffs and levels of maternal care in semel- and itero-parous females of the European earwig Forficula auricularia. Based on 15 traits measured in 494 females and their nymphs, our results revealed that iteroparous females laid their first clutch earlier, had more eggs in their first clutch, gained more weight during the 2 weeks following hatching of the first clutch, but produced eggs that developed more slowly than semelparous females. Among iteroparous females, the sizes of first and second clutches were significantly and positively correlated, indicating no investment trade-off between reproductive events. Iteroparous females also provided more food than semelparous ones, a result contrasting with predictions that iteroparity is incompatible with the evolution of maternal care. Finally, a controlled breeding experiment reported full mating compatibility among offspring from females of the two modes of parity, confirming that both types of females belong to one single species. Overall, these results indicate that alternative modes of parity represent coexisting life-history tactics that are likely to be condition-dependent and associated with offspring development and specific levels of maternal care in earwigs.     

Free and total cortisol levels in semelparous and iteroparous chinook salmon

Total cortisol, free cortisol and percent free cortisol were all significantly higher in semelparous male chinook salmon Oncorhynchus tshawytscha than in iteroparous and immature fish. The findings suggest that the regulation of both total and free cortisol concentrations may play key roles in mediating the post-spawning death of semelparous Pacific salmon.     

Histological assessment of organs in sexually mature and post-spawning steelhead trout and insights into iteroparity

Steelhead trout (Oncorhynchus mykiss) are anadromous and iteroparous, but repeat-spawning rates are generally low. Like other anadromous salmonids, steelhead trout fast during freshwater spawning migrations, but little is known about the changes that occur in vital organs and tissues. We hypothesized that fish capable of repeat-spawning would not undergo the same irreversible degeneration and cellular necrosis documented in semelparous salmon. Using Snake River steelhead trout as a model we used histological analysis to assess the cellular architecture in the pyloric stomach, ovary, liver, and spleen in sexually mature and kelt steelhead trout. We observed 38 % of emigrating kelts with food or fecal material in the gastrointestinal tract. Evidence of feeding was more likely in good condition kelts, and feeding was associated with a significant renewal of villi in the pyloric stomach. No vitellogenic oocytes were observed in sections of kelt ovaries, but perinucleolar and early/late stage cortical alveolus oocytes were present suggesting iteroparity was possible. We documented a negative correlation between the quantity of perinucleolar oocytes in ovarian tissues and fork length of kelts suggesting that larger steelhead trout may invest more into a single spawning event. Liver and spleen tissues of both mature and kelt steelhead trout had minimal cellular necroses. Our findings indicate that the physiological processes causing rapid senescence and death in semelparous salmon are not evident in steelhead trout, and recovery begins in fresh water. Future management efforts to increase iteroparity in steelhead trout and Atlantic salmon must consider the physiological processes that influence post-spawning recovery.     

The timing of spawning in capelin (Mallotus villosus Müller) at a coastal location in eastern Newfoundland

We tested three hypotheses concerning the timing of spawning for a circumpolar species, capelin (Mallotus villosus), for which timing of larval emergence is known to be synchronized by physical conditions. The first hypothesis, developed from previous studies, was that spawning would be synchronized by upwelling events. Initial results from Middle Cove Beach in eastern Newfoundland indicated that spawning was not synchronized with upwelling. We next hypothesized that spawning was a function of several environmental variables. Results from logistic regression indicated that neither single-factor nor multi-factor models could explain the timing of spawning. Single variables could predict spawning in some years but no variable could reliably predict the time of spawning year after year. Finally, we hypothesized that the probability of spawning increased as a set of significant variables approached preferred levels. For capelin at Middle Cove, the set of variables that influence capelin spawning were identified as wave height, sea surface roughness and capelin abundance in the water. Thus only a combination of variables explained the timing of spawning for capelin. Preferred conditions for capelin spawning were wave heights less than 20 cm at the beach, a sea surface with a slight ripple, and an intermediate rank abundance of capelin in the water corresponding to hundreds to thousands of individuals. Capelin abundance alone was not a useful predictor. During the course of the study we observed a shift in the dates that capelin arrived and spawned at the beach. During 1987–1990 capelin spawned at Middle Cove Beach during June, but in more recent years (1991–1993) capelin did not arrive or spawn until July.     

OPTIMAL REPRODUCTIVE EFFORT IN STOCHASTIC,DENSITY-DEPENDENT ENVIRONMENTS

The amount of effort organisms should put into reproducing at any given time has been a matter of debate for many years. Early models suggested a simple rule of thumb: iteroparity should be favored when juvenile survival is relatively variable and semelparity when adult survival is relatively variable. When more mathematically complex models were developed, these simple conclusions were found to be special cases. Variability can select toward iteroparity or semelparity depending on a number of factors irrespective of relative adult/juvenile survival (e.g, the density-independent models of Orzack and Tuljapurkar). Using new techniques, we estimate the ESS reproductive effort for stage-structured models in density-dependent and stochastic conditions. We find that variability causes significant changes in reproductive effort, these changes are often small (± 10% of determinstic ESS effort, but up to 50% change in some instances), and the amount that effort increases or decreases depends on many factors (e.g., the deterministic population dynamics, the vital rates affected by density, the amount of variation, the correlations between the vital rates, the distribution from which the variation is drawn, and the deterministic ESS effort). In a variable environment, semelparity is the ESS in only 3.5% of cases; iteroparity is the rule.     

TO AGE, TO DIE: PARITY, EVOLUTIONARY TRACKING AND COLE'S PARADOX

The existence of semelparity or "big bang" reproduction (reproducing only once in a lifetime) and iteroparity (reproducing more than once in a lifetime) has led to many questions investigating the evolution or persistence of these strategies. Here we investigate semelparity and iteroparity for their evolutionary importance. A mathematical model is used to illustrate how a population's ability to evolve depends on this life-history trait, and how this rate of evolution impacts the individual. We find that the ability of a trait to evolve is greater toward a semelparous strategy and this expresses a fitness advantage. This leads to an optimality between survival, population tracking ability, and lifetime fecundity.     

Assessing the Semelparity Hypothesis: Egg-guarding and Fecundity in the Malaysian Treehopper Pyrgauchenia tristaniopsis

According to the semelparity hypothesis, iteroparous insects should provide either no maternal care or less care than related semelparous species. We present field data on reproductive output and maternal care in the Southeast Asian treehopper Pyrgauchenia tristaniopsis (Mt. Kinabalu, Borneo) relevant to a preliminary assessment of the hypothesis. In a mark‐recapture experiment, more females than expected under semelparity were found to have oviposited a second clutch (37%). Female longevity was a of 75 d. Both these estimates were highly conservative. Oviposition was successive resulting in a of 46 eggs per clutch. Females provided care for eggs only, occasionally scraping their legs along the sides of the clutch apparently attempting to deter Brachygrammatella sp. egg parasitoids (Trichogrammatidae). Females straddled their clutch for a of 27 d, i.e. until 8 d after the beginning of first instar hatching. First instars hatched successively over a period of 11 d. When a female deserted her clutch, it contained about 37% yet unhatched eggs. Egg‐guarding effectively reduced egg mortality: the earlier a female was experimentally removed from her clutch the higher the egg mortality. Displacement experiments demonstrated that egg‐guarding is a behaviour actively maintained despite disturbances and specifically directed towards the egg clutch but not to the feeding site. We interpret our findings as being in accordance with the weaker claim of the semelparity hypothesis, i.e. the iteroparous P. tristaniopsis provided less maternal care than semelparous membracid species. Continued female feeding is discussed as a mechanism to display some level of care despite iteroparity.     

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.     

Beach Spawning in Fishes: Phylogenetic Tests of Hypotheses

Marine fishes that spawn at the water's edge or even out ofwater provide their eggs with the advantages of the warmer temperaturesand high oxygen availability of the high intertidal zone. However,they increase the risks of desiccation and terrestrial predation.Beach spawners are present in at least 6 families of teleostfishes. Two hypotheses about the origin of beach spawning aretested by mapping of reproductive habitat and spawning siteutilization onto phylogenies of two families that contain multiplespecies that spawn on beaches: Osmeridae, the smelts, and Atherinopsidae,the silversides. Our analysis suggests that beach spawning hasevolved repeatedly in certain lineages, and that its antecedentsare different for each family. Anadromy appears to have beenthe precursor for at least 3 different evolutionary originsof beach spawning in osmerids, while nearshore marine spawningin association with plant or gravel substrates was probablythe precursor for the atherinopsids. Phylogenetic analysis enablesus to reject or support specific evolutionary hypotheses foreach clade.     

Genetic diversity and differentiation in a wide ranging anadromous fish,American shad (Alosa sapidissima), is correlated with latitude

Studies that span entire species ranges can provide insight into the relative roles of historical contingency and contemporary factors that influence population structure and can reveal patterns of genetic variation that might otherwise go undetected. American shad is a wide ranging anadromous clupeid fish that exhibits variation in demographic histories and reproductive strategies (both semelparity and iteroparity) and provides a unique perspective on the evolutionary processes that govern the genetic architecture of anadromous fishes. Using 13 microsatellite loci, we examined the magnitude and spatial distribution of genetic variation among 33 populations across the species' range to (i) determine whether signals of historical demography persist among contemporary populations and (ii) assess the effect of different reproductive strategies on population structure. Patterns of genetic diversity and differentiation among populations varied widely and reflect the differential influences of historical demography, microevolutionary processes and anthropogenic factors across the species' range. Sequential reductions of diversity with latitude among formerly glaciated rivers are consistent with stepwise postglacial colonization and successive population founder events. Weak differentiation among U.S. iteroparous populations may be a consequence of human‐mediated gene flow, while weak differentiation among semelparous populations probably reflects natural gene flow. Evidence for an effect of reproductive strategy on population structure suggests an important role for environmental variation and suggests that the factors that are responsible for shaping American shad life history patterns may also influence population genetic structure.     

Thermohaline tolerance and embryonic development in capelin eggs (Mallotus villosus) from the Northeast Atlantic Ocean

Capelin (Mallotus villosus) displays alternative reproductive modes throughout its circumpolar distribution. This predicts divergent thermohaline tolerance of eggs because they are incubated in either a steady offshore or variable intertidal environment. We investigate herein thermohaline tolerance of eggs from the offshore spawning Barents Sea capelin. Subsequently, we compare our data with those previously published on other offshore and intertidal spawning capelin populations across the Northeast Atlantic Ocean, with the aim of determining possible patterns in the thermohaline tolerance of eggs from the alternative reproductive modes. In a 2?×?4 factorial design various combinations of salinities and temperatures had only negligible effect on the survival of eggs until first hatch. The embryonic development rate from fertilisation until first hatch across populations and between the two reproductive modes suggested non-local thermohaline tolerance towards the physical factors during development. Finally, no differences were observed in salinity tolerance from fertilisation to first hatch between populations representing different reproductive modes. The present findings demonstrate wide thermohaline tolerance of capelin eggs regardless of population origin and reproductive mode.     

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.