Effects of parental survival on clutch size decisions in fluctuating environments

Whereas in constant environments parental survival has no effect on optimal clutch size in the absence of trade-offs between juvenile and parental survival, the situation is drastically different in fluctuating environments. We consider a model in which, with respect to reproduction, parents and offspring are equivalent at the start of the next breeding season. When generations are non-overlapping, the clutch size maximizing geometric mean surviving number of offspring is optimal among all pure clutch size strategies. We prove that, as parental survival increases relative to that of the offspring, the optimal clutch size converges to the arithmetic mean maximizing clutch size (the so-called ‘Lack clutch size’). We also give a numerical procedure for calculating optimal mixed strategies and we show that, as environmental variance increases and/or parental survival decreases, mixed rather than pure strategies become optimal. Furthermore, we explain how to estimate fitness from empirical data under the assumptions of our model. This revised version was published online in July 2006 with corrections to the Cover Date.     

Implicit frequency dependence and kin selection in fluctuating environments

Summary I consider a general model of a fluctuating environment in which the environmental state each year is drawn at random from some given distribution. Each year organisms must choose what action to perform before the environmental state for that year is known. There is no interaction with kin. In this scenario, natural selection will tend to produce organisms which maximize their geometric mean fitness. In this paper I introduce the idea of the profile of a strategy. This function quantifies how the strategy peforms for each environmental state. I show that there is a unique profile such that a strategy is optimal if and only if it has this profile. I then give a characterization of the optimal profile which generalizes previous work by others in this area. The characterization of the optimal profile has a game theoretical interpretation. Motivated by this I introduce a game in which individuals play the field in a constant environment. This game may be interpreted as a cooperative game between kin. The key result of this paper shows that a strategy maximizes geometric mean fitness in the original fluctuating environment problem if and only if it is an evolutionarily stable strategy of the deterministic environment game. It is well known that an optimal strategy in a fluctuating environment may be mixed, involving adaptive coin-flipping. Others have previously noted that this may result in some individuals sacrificing individual reproductive success for the good of the genotype. My analysis shows that one may regain the concept of individual optimization if the quantity maximized is suitably defined. Under an optimal strategy every action taken maximizes the expected number of offspring produced, where this expectation is not calculated using the true distribution of environmental states, but a distribution modified to take account of the actions of kin.     

Phenotypic integration of life history and morphology: an example from three-spined stickleback, Gasterosteus aculeatus L.

Although typically life history and morphology are studied separately, they may evolve most often in concert. Therefore, a full understanding of the evolution of fish life-history patterns may require exploration of the evolutionary interplay between components of life history and other aspects of phenotype. One of the most promising approaches to understanding phenotypic integration is population comparison. This approach is particularly effective when ancestralderived relationships are understood and when multiple populations can be inferred to have evolved derived character states independently. Here we provide an example of this approach using five allopatric populations of freshwater three-spined stickleback ( Gasterosteus aculcatus L.) that have diverged in response to differences in selection regimes among the lakes they inhabit. We demonstrate a relationship between one aspect of reproductive life history, clutch volume and relative body shape. The differences are consistent with those predicted on the basis of differences in trophic habit and overall body form. Finally, we discuss the value of particular groups of fish for use in comparative studies and explore the kinds of evolutionary issues that can be addressed through population comparison.     

Life history evolution in cichlids 2: directional evolution of the trade-off between egg number and egg size

The negative relationship between offspring number and offspring size provides a classic example of the role of trade-offs in life history theory. However, the evolutionary transitions in egg size and clutch size that have produced this negative relationship are still largely unknown. Since body size may affect both of these traits, it would be helpful to understand how evolutionary changes in body size may have facilitated or constrained shifts in clutch and egg size. By using comparative methods with a database of life histories and a phylogeny of 222 genera of cichlid fishes, we investigated the order of evolutionary transitions in these traits in relation to each other. We found that the ancestral large-bodied cichlids first increased egg size, followed by a decrease in both body size and clutch size resulting in the common current combination of a small-bodied cichlid with a small clutch of large eggs. Furthermore, lineages that deviated from the negative relationship between clutch and egg size underwent different transitions in these traits according to their body size (large bodied genera have moved towards the large clutch/small egg end of the continuum and small bodied genera towards the small clutch/large egg end of the continuum) to reach the negative relationship between clutch size and egg size. Our results show that body size is highly important in shaping the negative relationship between clutch size and egg size.     

Clutch size and the costs of incubation in the house wren

Trade-offs in the allocation of finite resources among differentstages of a breeding attempt as well as between different reproductiveevents should shape the evolution of life-history traits. Toinvestigate the effects of incubation effort on within-broodand between-brood trade-offs in house wrens (Troglodytes aedon),we manipulated the clutch size that females incubated. We isolatedeffects of incubation by reversing the manipulation at hatchingto allow all parents to provision their natural brood sizes.Females that incubated enlarged clutches had longer incubationperiods than control females, both early and late in the season,suggesting that the experimental treatment increased incubationeffort. Contrary to predictions, however, increased incubationeffort did not adversely affect the allocation of effort tonestling provisioning. Rather, in the early season, but notin the late season, females that incubated enlarged clutchesappeared to allocate more effort to nestling provisioning, producingheavier and larger fledglings than control females. Althoughfemales with enlarged early-season clutches consequently lostmore mass than control females, this was likely an adaptiveresponse to reduce wing loading in anticipation of high provisioningdemands. There were no treatment-related differences in fledglingmass or size, or in female mass loss, in the late season. Thus,elevated incubation demands negatively affected a fitness-relatedtrait (duration of incubation) that may constrain clutch sizebut not the allocation of resources to subsequent stages ofthe same breeding event or to subsequent breeding events. Wesuggest that environmental conditions may mediate clutch-sizeeffects on trade-offs in allocation of resources between incubationand nestling provisioning.     

Biochemical and egg size evolution of freshwater fishes in the Rhinogobius brunneus complex (Pisces, Gobiidae) in Okinawa, Japan

Many colour morphs have been recognized in the Rhinogobius brunneus complex. A recent electrophoretic study has revealed that some of the colour morphs are well differentiated from each other genetically. In Okinawa, egg-size and life-history variation has been found in addition to the colour variation in this species complex. To clarify the nature of this life-history variation, gobies of a fluviatile morph with large eggs as well as three other amphidromous morphs with small eggs, inhabiting a single stream sympatrically in Okinawa, were analysed by electrophoresis and the females were also used for comparison of egg and clutch sizes. Electrophoretic data for 34 loci showed that each morph was separated by a fixed-allele difference for at least one locus, indicating that the four morphs which occurred sympatrically are reproductively isolated from each other. However, Nei's genetic distance between the fluviatile morph and one of the amphidromous morphs was much smaller (0.026) than distances among amphidromous gobies (0.323-0.480). Egg size of the former was by far the largest among the four. These results imply that speciation of the fluviatile morph accompanied by the egg-size increase has been completed rapidly without considerable genetic differentiation.     

The evolution of life histories in spatially heterogeneous environments: Optimal reaction norms revisited

Summary Natural populations live in heterogeneous environments, where habitat variation drives the evolution of phenotypic plasticity. The key feature of population structure addressed in this paper is the net flow of individuals from source (good) to sink (poor) habitats. These movements make it necessary to calculate fitness across the full range of habitats encountered by the population, rather than independently for each habitat. As a consequence, the optimal phenotype in a given habitat not only depends on conditions there but is linked to the performance of individuals in other habitats. We generalize the Euler-Lotka equation to define fitness in a spatially heterogeneous environment in which individuals disperse among habitats as newborn and then stay in a given habitat for life. In this case, maximizing fitness (the rate of increase over all habitats) is equivalent to maximizing the reproductive value of newborn in each habitat but not to maximizing the rate of increase that would result if individuals in each habitat were an isolated population. The new equation can be used to find optimal reaction norms for life history traits, and examples are calculated for age at maturity and clutch size. In contrast to previous results, the optimal reaction norm differs from the line connecting local adaptations of isolated populations each living in only one habitat. Selection pressure is higher in good and frequent habitats than in poor and rare ones. A formula for the relative importance of these two factors allows predictions of the habitat in which the genetic variance about the optimal reaction norm should be smallest.     

Clutch size in parasitoids: the egg production rate as a constraint

Summary In many species of insect parasitoids, adult females mature eggs as they search their environment for hosts. In such species, the number of mature eggs, at the point of finding a host, is a function of the interhost time and the rate of egg maturation. Assuming that interhost search times are variable, we use a version of the marginal value theorem to derive a decision rule for optimizing the time spent exploiting individual hosts; this indirectly determines clutch size. We find that a threshold search time exists above which a female should simply lay her currently mature eggs and depart from the host. However, when the search time has been less than the threshold, a female should oviposit, but then remain on the host to mature and lay additional eggs, until the threshold time is reached.     

Context-dependent sexual advertisement: plasticity in development of sexual ornamentation throughout the lifetime of a passerine bird

Male investment into sexual ornamentation is a reproductive decision that depends on the context of breeding and life history state. In turn, selection for state- and context-specific expression of sexual ornamentation should favour the evolution of developmental pathways that enable the flexible allocation of resources into sexual ornamentation. We studied lifelong variation in the expression and condition-dependence of a sexual ornament in relation to age and the context of breeding in male house finches (Carpodacus mexicanus)--a species that develops a new sexual ornament once a year after breeding. Throughout males' lifetime, the elaboration of ornamentation and the allocation of resources to the development of sexual ornamentation depended strongly on pairing status in the preceding breeding season--males that were single invested more resources into sexual ornamentation and changed ornamentation more than males that were paired. During the initial (post-juvenile) moult, the expression of ornamentation was closely dependent on individual condition, however the condition-dependence of ornamentation sharply decreased throughout a male's lifetime and in older males expression of sexual ornamentation was largely independent of condition during moult. Selection for early breeding favoured greater ornamentation in males that were single in the preceding seasons and the strength of this selection increased with age. On the contrary, the strength of selection on sexual ornamentation decreased with age in males that were paired in the preceding breeding season. Our results reveal strong context-dependency in investment into sexual ornamentation as well as a high flexibility in the development of sexual ornamentation throughout a male's life.     

Selection in a fluctuating environment leads to decreased genetic variation and facilitates the evolution of phenotypic plasticity

Changes in the environment are expected to induce changes in the quantitative genetic variation, which influences the ability of a population to adapt to environmental change. Furthermore, environmental changes are not constant in time, but fluctuate. Here, we investigate the effect of rapid, continuous and/or fluctuating temperature changes in the seed beetle Callosobruchus maculatus, using an evolution experiment followed by a split-brood experiment. In line with expectations, individuals responded in a plastic way and had an overall higher potential to respond to selection after a rapid change in the environment. After selection in an environment with increasing temperature, plasticity remained unchanged (or decreased) and environmental variation decreased, especially when fluctuations were added; these results were unexpected. As expected, the genetic variation decreased after fluctuating selection. Our results suggest that fluctuations in the environment have major impact on the response of a population to environmental change; in a highly variable environment with low predictability, a plastic response might not be beneficial and the response is genetically and environmentally canalized resulting in a low potential to respond to selection and low environmental sensitivity. Interestingly, we found greater variation for phenotypic plasticity after selection, suggesting that the potential for plasticity to evolve is facilitated after exposure to environmental fluctuations. Our study highlights that environmental fluctuations should be considered when investigating the response of a population to environmental change.     

The question of fluctuating asymmetry in the blacklegged tick Ixodes scapularis (Acari: Ixodidae)

An analysis of fluctuating asymmetry was conducted on populations of the blacklegged tick Ixodes scapularis. The eight groups used in this study consisted of larvae and nymphs and males and females from the states of Minnesota, Massachusetts, Maryland, Missouri, North Carolina and Georgia and the F1 progenies of reciprocal crosses between ticks from Massachusetts and Georgia. Measurements included 16 larval, 19 nymphal, ten female and 12 male bilateral characters. Only five differences between the right and left bilateral characters had normal distributions with means of zero and differences in variances between the groups. These five characters included three setal lengths of the larvae, the spiracular plate length of females and the coxa I internal spur widths of males. Bivariate plots of character size ((R+L)/2) and asymmetry (R-L) showed no correlation. In the spiracular plate lengths of females and one of the setal lengths, ticks from Massachusetts had significantly less within-group variance than all the other groups. The only character in which fluctuating asymmetry was observed was the coxa I internal spur width of males, in which ticks from Minnesota, Missouri and North Carolina had significantly greater variance than the remaining groups; fluctuating asymmetry in this character may be explained by sexual selection. The cross progeny did not demonstrate any fluctuating asymmetry, as would be expected if the northern and southern forms of I. scapularis were true species. The virtual lack of fluctuating asymmetry in the characters used in this study further supports the conclusions of other studies which concluded that I. scapularis is a species with clinal variation and a broad geographic distribution.     

Salinity-linked growth in anguillid eels and the paradox of temperate-zone catadromy

Temperate-zone anguillid eels use both saline (marine or brackish) and fresh waters during their continental phase, but use of fresh waters is paradoxical because on average these fishes grow more rapidly in saline than in fresh waters. Based on data from anguillid eels whose habitat-residency histories had been determined by Sr:Ca otolithometry, superiority of growth rates in saline water is much greater in American eels Anguilla rostrata in north-eastern North America (mean saline:fresh growth rate ratio 2·07) than in European Anguilla anguilla , Japanese Anguilla japonica and shortfinned Anguilla australis eels (range of mean ratios 1·12–1·14). Data from A. rostrata in the Hudson Estuary, U.S.A., and Prince Edward Island, Canada, were used to test adaptive explanations of catadromous migrations. The hypothesis that lower mortality in fresh water offsets faster growth in saline water was not supported because loss (mortality + emigration ) rates did not vary between saline and fresh zones of the Hudson Estuary. Hypotheses that anguillid eels move to fresh water to escape from larger anguillid eels in saline water or to evaluate habitat quality were not supported by size and age distributions. Catadromy in temperate-zone anguillid eels increases the diversity of occupied habitats and therefore lowers fitness variance caused by environmental fluctuations. Catadromy in temperate-zone anguillid eels could be due to natural selection for maximum geometric mean fitness which is sensitive to fitness variance. Temperate-zone catadromy might also be maladaptive, at least in local areas, due to shifts over time in selective pressures or to inability of panmictic genetic systems to adapt to local conditions.     

Developmental instability in Brassica campestris (Cruciferae): fluctuating asymmetry of foliar and floral traits

The degree of fluctuating asymmetry of bilateral traits provides a measure of developmental instability, which can be influenced by genetic as well as environmental stress. We studied genetic variation between and within two populations of the mustard Brassica campestris for asymmetry of foliar (cotyledon width) and floral (petal length and width) traits as well as for phenological (germination and flowering) and performance (biomass and flowering) traits. The two populations differed in mean expression of most traits, including asymmetry. However, within-population estimates of genetic variability tended to be lower for asymmetry than other traits. Asymmetry was greater in the population that had lower biomass accumulation and flower production, which supports the idea that population-level asymmetry may be indicative of population-level performance. However, within each population, evidence that performance was negatively correlated with asymmetry was equivocal. Within populations there was little or no concordance among estimates of asymmetry based on different structures, i.e., plants that had highly asymmetrical cotyledons did not tend to have highly asymmetrical petals. The lack of a general buffering capacity at the individual level may be explained by developmental processes (e.g., action of different genes or morphogens) as well as evolutionary processes (e.g., selection on asymmetry of different traits).     

The causes and consequences of variation in offspring size: a case study using Daphnia

Offspring size can have large and direct fitness implications, but we still do not have a complete understanding of what causes offspring size to vary. Daphnia (water fleas) generally produce fewer and larger offspring when food is limited. Here, we use a mathematical model to show that this could be explained by either: (1) an advantage of producing larger eggs when food is limited; or (2) a lower boundary on egg volume (below which eggs do not have sufficient resources to be viable), that is similar in volume to the evolutionarily stable egg volume predicted by standard clutch size models. We tested the first possibilities experimentally by placing offspring from mothers kept at two food treatments (high and low - leading to relatively small and large eggs respectively) into two food treatments (same as maternal treatments, in a fully factorial design) and measuring their fitness (reproduction, age at maturity, and size at maturity). We also tested survival under starvation conditions of offspring produced from mothers at low and high food treatments. We found that (larger) offspring produced by low-food mothers actually had lower fitness as they took longer to reproduce, regardless of their current food treatment. Additionally, we found no survival advantage to being born of a food-stressed mother. Consequently, our results do not support the hypothesis that there is an advantage to producing larger eggs when food is limited. In contrast, data from the literature support the importance of a lower boundary on egg size.     

The consequences of adult foraging success on the components of lifetime fitness in a semelparous,sit and wait predator

Summary We evaluated the role of adult foraging success in the lifetime fitness of female crab spidersMisumena vatia. Misumena are semelparous, sit and wait predators that hunt for insect prey on flowers, in this study primarily on inflorescences (umbels) of milkweedAsclepias syriaca. We used path analysis to integrate previously performed experimental and observational studies, thereby establishing the magnitude, correlations and causal relationships of key foraging and life history variables and their roles in lifetime fitness. A path proceeding from maternal hunting patch choice through maternal mass, clutch mass and number of dispersal-age young was the dominant element and explained a large part of the variation. Other paths that incorporated parasitism of the egg mass and predation of young leaving the nests made only small impacts on variation. No trade-offs were found, primarily because a single factor, maternal mass (a maternal effect) resulting from foraging success, provided major benefits for successive life history stages. Since differences in the numbers of eggs, egg loss and mortality at dispersal resulted almost entirely from differences in maternal mass, they are controlled by the maternal generation and, thus, are appropriately attributed to the lifetime fitnesses of the mothers, rather than to those of their offspring.