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.     

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.     

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.     

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).     

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.     

The evolution of offspring size and number: a test of the Smith-Fretwell model in three species of crickets

Most models of parental investment in offspring assume a trade-off between propagule size and number, and an increasing concave down function relating offspring fitness to propagule size. In this study, we test these two fundamental assumptions, using three closely related species of crickets, Gryllus firmus, G. veletis, and G. pennsylvanicus. Egg weight, 35-day fecundity and 35-day egg biomass were estimated in a population of each species, and the relationships between these reproductive traits and date of egg laying and body size were estimated. The relationships between egg weight and offspring survival were also sought for eggs buried at different depths, soil moistures, and soil types (G. firmus and G. veletis), as well as in the field (G. pennsylvanicus). A trade-off between egg weight and 35-day fecundity was revealed in a multivariate analysis taking into account among-species variation in egg weight and body size. Independent of the environmental conditions affecting the eggs, a positive correlation existed between the number of larvae that emerged from the soil and propagule weight in each species. Therefore, these findings provide partial support for the assumptions considered in the models mentioned above. A single optimal egg size was favored in two out of the three sets of conditions in which the functions relating egg weight to larval survival could be derived. The conditions encountered by the eggs, however, influenced the average survival of the larvae, as well as the shape of the relationship between egg weight and offspring survival. This suggests that cricket eggs frequently face heterogeneous environments with respect to egg and hatchling survival; the implication of habitat heterogeneity on the evolution of an optimal egg size is considered. The relationships between the reproductive components and female age and size, as well as between egg size and variation in cricket life-history, are discussed in an ecological and evolutionary context.     

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.     

Seasonal variation of egg size and number in a Daphnia pulex population

Seasonal variation of egg size and number was examined in a Daphnia pulex population inhabiting a vernal pond. In this population, size at maturity declines at midseason, probably as an adaptive response to size-selective predation by larvae of the salamander Ambystoma. The larger early season individuals produce more and larger eggs than the smaller late season individuals. Age at maturity does not vary between seasons. Laboratory experiments indicate that temperature may affect egg size, egg number and size at maturity. However, field data suggest that temperature accounts for only a small fraction of the total variation in egg size and number. Indirect measures of nutrition indicate that food limitation does not cause the seasonal decline in egg size and number. The seasonal change in reproductive traits is well correlated with changes in invertebrate and vertebrate predation. Examination of predator feeding preferences and their impact on Daphnia mortality indicate that variation of reproductive traits is most likely a complex adaptation to changing predation regimes.     

Propagule size and parental care: the "safe harbor" hypothesis

Species that protect their offspring (by egg-brooding or live-bearing) produce larger (and hence fewer) propagules than do related species that do not protect their offspring. This result holds true in most animal groups showing parental care. Analysis of these data supports the hypothesis that propagule size evolves in response to relative survivorship rates during and after the propagule stage: natural selection is most likely to favor large egg size when the egg is a safe harbor.     

宁波滑蜥两性异形和雌性繁殖

蜥蜴的雌性繁殖特征对理解两性异形的进化原因起着重要作用。于2011年4月在安徽滁州采集宁波滑蜥(Scincella modesta),定量研究该种形态特征的两性异形和雌性繁殖特征,检验成体形态特征两性异形与雌性繁殖的相关性。研究共采集43条(17♀♀,26♂♂)宁波滑蜥,雄性和雌性个体的最大体长分别为47.4 mm和46.6 mm。雌雄两性在体长和头宽上没有差异,而在腹长和头长上差异显著,雄性有较大的头长,雌性有较大的腹长。宁波滑蜥年产单窝卵。窝卵数和窝卵重与雌体体长及腹长呈正相关,卵重与雌体体长无相关性。窝卵数及卵重的变异系数分别为0.20和0.12。卵长径与窝卵数呈负相关,而卵短径与窝卵数无关。雌体主要通过增加窝卵数来增加繁殖输出。这些结果表明,宁波滑蜥是雌雄个体大小同形的两性异形模式,性选择使得雄性有着较大的头长,以具有较高的交配成功率,生育力选择使得雌性有着较大的腹长,以具有较大的生育力和繁殖输出。     

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.     

Egg-size variation in the bluethroat (Luscinia s. svecica): constraints and adaptation

We examined inter- and intra-clutch egg-size variation in the bluethroat (Luscinia s. svecica), an open-nesting passerine breeding in the sub-alpine region in southern Norway. By removing first clutches shortly after egg-laying, we induced laying of a repeat clutch. Females significantly reduced the number of eggs from the first to the second nesting attempt, but increased mean egg size. Females in good condition laid significantly larger eggs than those in poor condition. Consistent with predictions of the brood survival hypothesis, assuming an adaptive investment in last eggs to ensure survival of all eggs in the clutch, we found that the size of the last eggs in first clutches was generally larger than the mean egg size of the clutch, and that the relative size of the last egg increased with clutch size. However, a large last egg reflected a general increase in egg size throughout the laying sequence rather than a specific investment in the last egg only. Egg size was not significantly influenced by sex or paternity (within-pair versus extra-pair) of the embryo. In repeat clutches the last egg was not consistently larger than the mean for the clutch. We conclude that female bluethroats face resource limitations during egg formation early in the season, and that the patterns of increase in egg size with laying order for first clutches, and from first to repeat clutches, can largely be explained by proximate constraints on egg formation.     

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.     

Comparative analysis of phylogenetic and fishing effects in life history patterns of teleost fishes

The effects of fishing on life history traits and life history strategies of teleost fishes are analysed by a new comparative method that splits traits into an allometric part (size effect), an autoregressive phylogenetic component, and an environmental component (fishing effect). Both intra- and inter-specific variation of age and size at maturity, fecundity, adult size and egg size are analysed by comparing 84 populations of 49 species submitted to various fishing pressures. Two axes of life history diversification are found among teleosts. One is the well-known slow-fast continuum separating short-lived and early maturing species (like Clupeiformes) from longer-lived species that mature late relative to their size and spawn larger eggs (like salmonids or Scorpaeniformes). An additional strategy involves the schedule of resource allocation to growth and reproduction. Indeterminate growth allows higher teleosts (e.g. Gadiformes) to reach a large size while maturing early and laying small eggs. Increasing fishing pressure decreases age at maturity and egg size, and increases fecundity at maturity, the slope of the fecundity-length relationship and relative size at maturity. These compensations for higher adult mortality differ among life history strategies. Indeterminate growth is associated with a greater flexibility in resource allocation to growth and reproduction that facilitates greater resilience to fishing mortality.     

COOPERATIVE BREEDING FAVORS MATERNAL INVESTMENT IN SIZE OVER NUMBER OF EGGS IN SPIDERS

The transition to cooperative breeding may alter maternal investment strategies depending on density of breeders, extent of reproductive skew, and allo‐maternal care. Change in optimal investment from solitary to cooperative breeding can be investigated by comparing social species with nonsocial congeners. We tested two hypotheses in a mainly semelparous system: that social, cooperative breeders, compared to subsocial, solitarily breeding congeners, (1) lay fewer and larger eggs because larger offspring compete better for limited resources and become reproducers; (2) induce egg size variation within clutches as a bet‐hedging strategy to ensure that some offspring become reproducers. Within two spider genera, Anelosimus and Stegodyphus, we compared species from similar habitats and augmented the results with a mini‐meta‐analysis of egg numbers depicted in phylogenies. We found that social species indeed laid fewer, larger eggs than subsocials, while egg size variation was low overall, giving no support for bet‐hedging. We propose that the transition to cooperative breeding selects for producing few, large offspring because reproductive skew and high density of breeders and young create competition for resources and reproduction. Convergent evolution has shaped maternal strategies similarly in phylogenetically distant species and directed cooperatively breeding spiders to invest in quality rather than quantity of offspring.     

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.     

Evolutionary ecology of egg size and number in a seed beetle: genetic trade-off differs between environments

Abstract In many organisms, large offspring have improved fitness over small offspring, and thus their size is under strong selection. However, due to a trade-off between offspring size and number, females producing larger offspring necessarily must produce fewer unless the total amount of reproductive effort is unlimited. Because differential gene expression among environments may affect genetic covariances among traits, it is important to consider environmental effects on the genetic relationships among traits. We compared the genetic relationships among egg size, lifetime fecundity, and female adult body mass (a trait linked to reproductive effort) in the seed beetle, Stator limbatus , between two environments (host-plant species Acacia greggii and Cercidium floridum ). Genetic correlations among these traits were estimated through half-sib analysis, followed with artificial selection on egg size to observe the correlated responses of lifetime fecundity and female body mass. We found that the magnitude of the genetic trade-off between egg size and lifetime fecundity differed between environments–a strong trade-off was estimated when females laid eggs on C. floridum seeds, yet this trade-off was weak when females laid eggs on A. greggii seeds. Also differing between environments was the genetic correlation between egg size and female body mass–these traits were positively genetically correlated for egg size on A. greggii seeds, yet uncorrelated on C. floridum seeds. On A. greggii seeds, the evolution of egg size and traits linked to reproductive effort (such as female body mass) are not independent from each other as commonly assumed in life-history theory.     

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.     

A comparative study of egg mass and clutch size in the Anseriformes

The factors explaining interspecific differences in clutch investment in precocial birds are poorly understood. We investigated how variations in clutch characteristics are related to environmental factors in a comparative study of 151 extant species of ducks, geese and swans (Anseriformes). Egg mass was negatively related to clutch size in a phylogenetic regression, a relationship that was much stronger when controlling for female mass. Nest placement was related to both egg size and clutch size, with cavity-nesting species laying more but smaller eggs. Egg size was positively correlated with incubation period and with female mass, and also with sexual size dimorphism (i.e. male mass relative to that of the female). Clutch size was not related to female mass. Species with long term pair bonds laid smaller clutches and larger eggs. The size of the breeding range was strongly positively correlated with clutch size and clutch mass, and its inclusion in multivariate models made other biogeographical variables (hemisphere, breeding latitude or insularity) non-significant. The small clutches in insular species appear to be a product of small range size rather than insularity per se. Our results suggest there is an evolutionary trade-off between clutch and egg size, and lend support to Lack’s resource-limitation hypothesis for the waterfowl.     

Optimal size and number of propagules: allowance for discrete stages and effects of maternal size on reproductive output and offspring fitness

Existing optimality models of propagule size and number are not appropriate for many organisms. First, existing models assume a monotonically increasing offspring fitness/propagule size relationship. However, offspring survival during certain stages may decrease with increasing propagule size, generating a peaked offspring fitness/propagule size function (e.g., egg size in oxygen-limited aquatic environments). Second, existing models typically do not consider maternal effects on total reproductive output and the expression of offspring survival/propagule size relationships. However, larger females often have greater total egg production and may provide better habitats for their offspring. We develop a specific optimality model that incorporates these effects and test its predictions using data from salmonid fishes. We then outline a general model without assuming specific functional forms and test its predictions using data from freshwater fishes. Our theoretical and empirical results illustrate that, when offspring survival is negatively correlated with propagule size, optimal propagule size is larger in better habitats. When larger females provide better habitats, their optimal propagule size is larger. Nevertheless, propagule number should increase more rapidly than propagule size for a given increase in maternal size. In the absence of density dependence, females with greater relative reproductive output (i.e., for a given body size) should produce more but not larger propagules.