INTERACTIVE EFFECTS OF OFFSPRING SIZE AND TIMING OF REPRODUCTION ON OFFSPRING REPRODUCTION: EXPERIMENTAL,MATERNAL, AND QUANTITATIVE GENETIC ASPECTS

We demonstrate that egg size in side-blotched lizards is heritable (parent-offspring regressions) and thus will respond to natural selection. Because our estimate of heritability is derived from free-ranging lizards, it is useful for predicting evolutionary response to selection in wild populations. Moreover, our estimate for the heritability of egg size is not likely to be confounded by nongenetic maternal effects that might arise from egg size per se because we estimate a significant parent-offspring correlation for egg size in the face of dramatic experimental manipulation of yolk volume of the egg. Furthermore, we also demonstrate a significant correlation between egg size of the female parent and clutch size of her offspring. Because this correlation is not related to experimentally induced maternal effects, we suggest that it is indicative of a genetic correlation between egg size and clutch size. We synthesize our results from genetic analyses of the trade-off between egg size and clutch size with previously published experiments that document the mechanistic basis of this trade-off. Experimental manipulation of yolk volume has no effect on offspring reproductive traits such as egg size, clutch size, size at maturity, or oviposition date. However, egg size was related to offspring survival during adult phases of the life history. We partitioned survival of offspring during the adult phase of the life history into (1) survival of offspring from winter emergence to the production of the first clutch (i.e., the vitellogenic phase of the first clutch), and (2) survival of the offspring from the production of the first clutch to the end of the reproductive season. Offspring from the first clutch of the reproductive season in the previous year had higher survival during vitellogenesis of their first clutch if these offspring came from small eggs. We did not observe selection during these prelaying phases of adulthood for offspring from later clutches. However, we did find that later clutch offspring from large eggs had the highest survival over the first season of reproduction. The differences in selection on adult survival arising from maternal effects would reinforce previously documented selection that favors the production of small offspring early in the season and large offspring later in the season—a seasonal shift in maternal provisioning. We also report on a significant parent-offspring correlation in lay date and thus significant heritable variation in lay date. We can rule out the possibility of yolk volume as a confounding maternal effect—experimental manipulation of yolk volume has no effect on lay date of offspring. However, we cannot distinguish between genetic effects (i.e., heritable) and nongenetic maternal effects acting on lay date that arise from the maternal trait lay date per se (or other unidentified maternal traits). Nevertheless, we demonstrate how the timing of female reproduction (e.g., date of oviposition and date of hatching) affect reproductive attributes of offspring. Notably, we find that date of hatching has effects on body size at maturity and fecundity of offspring from later clutches. We did not detect comparable effects of lay date on offspring from the first clutch.     

EXTREME SELECTION ON SIZE IN THE EARLY LIVES OF FISH

Although fitness typically increases with body size and selection gradients on size are generally positive, much of this information comes from terrestrial taxa. In the early life history of fish, there is evidence of selection both for and against larger size, leaving open the question of whether the general pattern for terrestrial taxa is valid for fish. We reviewed studies of size‐dependent survival in the early life history of fish and obtained estimates of standardized selection differentials from 40 studies. We found that 77% of estimated selection differentials favored larger size and that the strength of selection was more than five times that seen in terrestrial taxa. Selection decreased with study period duration and initial length, and disruptive selection occurred significantly more frequently than stabilizing selection. Contrary to expectations from Bergmann's rule, selection on size did not increase with latitude.     

CONSTRAINTS ON THE ADULT‐OFFSPRING SIZE RELATIONSHIP IN PROTISTS

The relationship between adult and offspring size is an important aspect of reproductive strategy. Although this filial relationship has been extensively examined in plants and animals, we currently lack comparable data for protists, whose strategies may differ due to the distinct ecological and physiological constraints on single‐celled organisms. Here, we report measurements of adult and offspring sizes in 3888 species and subspecies of foraminifera, a class of large marine protists. Foraminifera exhibit a wide range of reproductive strategies; species of similar adult size may have offspring whose sizes vary 100‐fold. Yet, a robust pattern emerges. The minimum (5th percentile), median, and maximum (95th percentile) offspring sizes exhibit a consistent pattern of increase with adult size independent of environmental change and taxonomic variation over the past 400 million years. The consistency of this pattern may arise from evolutionary optimization of the offspring size‐fecundity trade‐off and/or from cell‐biological constraints that limit the range of reproductive strategies available to single‐celled organisms. When compared with plants and animals, foraminifera extend the evidence that offspring size covaries with adult size across an additional five orders of magnitude in organism size.     

FEMALE PROMISCUITY AND MATERNALLY DEPENDENT OFFSPRING GROWTH RATES IN MAMMALS

Conflicts between family members are expected to influence the duration and intensity of parental care. In mammals, the majority of this care occurs as resource transfer from mothers to offspring during gestation and lactation. Mating systems can have a strong influence on the severity of familial conflict—where female promiscuity is prevalent, conflict is expected to be higher between family members, causing offspring to demand more resources. If offspring are capable of manipulating their mothers and receive resources in proportion to their demands, resource transfer should increase with elevated promiscuity. We tested this prediction, unexplored across mammals, using a comparative approach. The total durations of gestation and lactation were not related to testes mass, a reliable proxy of female promiscuity across taxa. Offspring growth during gestation, however, and weaning mass, were positively correlated with testes mass, suggesting that offspring gain resources from their mothers at faster rates when familial conflict is greater. During gestation, the relationship between offspring growth and testes mass was also related to placenta morphology, with a stronger relationship between testes mass and growth observed in species with a less invasive placenta. Familial conflict could have a pervasive influence on patterns of parental care in mammals.     

MATERNAL INHERITANCE OF CONDITION AND CLUTCH SIZE IN THE COLLARED FLYCATCHER

Maternal effects may strongly influence evolutionary response to natural selection but they have been little studied in the wild. We use a novel combination of experimental and statistical methods to estimate maternal effects on condition and clutch size in the collared flycatcher, where we define “condition” to be the nongenetic component of clutch size. We found evidence of two maternal effects. The first (m) was the negative effect of mother's clutch size on daughter's condition, when mother's condition was held constant. The second (M) was the positive effect of mother's condition on daughter's condition, when mother clutch size was held constant. These two effects oppose one another because mothers in good condition also lay many eggs. The maternal effects were large: Experimentally adding an egg to a mother's nest reduced clutch sizes of her daughters by 1/4 egg (i.e., m = -0.25). Measured degree of resemblance between mother and daughter clutch sizes yielded M = 0.43. The results weakly support the presence of heritable genetic variation in clutch size: additive genetic variance/total phenotypic variance = 0.33. This estimate was highly variable probably because, as we show, mother-daughter resemblance may depend hardly at all on the amount of genetic variance when maternal effects are present. Daughter-mother regression (a standard method for estimating heritability) is consequently a poor guide to the amount of genetic variance in clutch size. Our results emphasize the value of combining field experiments with observations for studying inheritance.     

ADAPTIVE MATERNAL ADJUSTMENTS OF OFFSPRING SIZE IN RESPONSE TO CONSPECIFIC DENSITY IN TWO POPULATIONS OF THE LEAST KILLIFISH, HETERANDRIA FORMOSA

Given a trade-off between offspring size and number and an advantage to large size in competition, theory predicts that the offspring size that maximizes maternal fitness will vary with the level of competition that offspring experience. Where the strength of competition varies, selection should favor females that can adjust their offspring size to match the offspring's expected competitive environment. We looked for such phenotypically plastic maternal effects in the least killifish, Heterandria formosa , a livebearing, matrotrophic species. Long-term field observations on this species have revealed that some populations experience relatively constant, low densities, whereas other populations experience more variable, higher densities. We compared sizes of offspring born to females exposed during brood development to either low or high experimental densities, keeping the per capita food ration constant. We examined plastic responses to density for females from one population that experiences high and variable densities and another that experiences low and less-variable densities. We found that, as predicted, female H. formosa produced larger offspring at the higher density. Unexpectedly, we found similar patterns of plasticity in response to density for females from both populations, suggesting that this response is evolutionarily conserved in this species.     

THE INTENSITY OF SELECTION ACTING ON THE COUCH POTATO GENE—SPATIAL–TEMPORAL VARIATION IN A DIAPAUSE CLINE

Cosmopolitan populations of Drosophila melanogaster have co‐opted a form of reproductive diapause to overwinter in northern populations. Polymorphism in the couch potato gene has been implicated in genetic variation for this diapause trait. Using a collection of 20 populations from Florida to Canada and 11 collections from 3 years in a Pennsylvania orchard, we estimated the allele frequencies for 15 single nucleotide polymorphisms (SNPs) in the couch potato gene. These include the specific polymorphism associated with diapause inducability. We find that the SNP polymorphism, 48034(A/T), is correlated with latitude and its frequencies are predicted by the incidence of diapause trait. We find that the clinal patterns for cpo SNPs sampled in 1997 are similar to the same SNPs sampled in 2009–2010. SNPs that show apparent associations with cpo expression are also clinal with the low‐expression allele increasing in frequency, as would be predicted from functional knockout studies of cpo. Finally, we see a significant pattern where the frequency of the diapause‐causing allele drops in frequency during the summer season, consistent with the drop in the incidence of the diapause trait. The selection required to drive this response is large, roughly 24% to 59% per generation depending on the degree of dominance.     

SPATIAL AND TEMPORAL VARIATION IN SELECTION ON CORRELATED LIFE-HISTORY TRAITS AND PLANT SIZE IN CHAMAECRISTA FASCICULATA

Intraspecific studies of selection on multiple traits of a plant's life history provide insight as to how the composite life history of an organism evolves. Current understanding of selection on plant life-history traits is deficient in three important areas: 1) the effects of selection through correlated traits, 2) the effects of selection on a trait throughout the plant's lifetime, and 3) spatial and temporal variation in selection on plant life-history traits among populations and years. This study documents spatial and temporal variation in selection on three life-history and two morphological traits for two natural populations of Chamaecrista fasciculata, a native summer annual. Life-history and morphological traits (date of seedling emergence, size at establishment, size prior to reproduction, date of initial flowering, and date of initial fruit maturation) varied significantly between sites and/or years. Selection on traits varied either spatially, between sites and among transects within one site, or temporally, between years. In addition, life-history traits were phenotypically correlated among themselves and with morphological traits; correlations were generally constant over time and space. Indirect selection caused changes in means and variances in traits not under direct selection, but which were correlated with traits under selection. Selection on date of emergence varied in direction and magnitude among different life-cycle stages, while selection on other traits varied only in magnitude among life stages of the plant. This study documents the complexity of the selective process and the importance of considering multiple life stages and traits when studying the evolution of life-history traits.     

NATURAL SELECTION ON BODY SIZE AND LAYING DATE IN THE TREE SWALLOW

I measured natural selection on body size and laying date in a population of tree swallows (Tachycineta bicolor) from 1986 to 1988. There was little evidence of selection on body size associated with overwinter survival. Disruptive selection on tarsus length, associated with female reproductive success, was detected in one of three years. Both repeatability and mother-daughter regression suggested that laying date was heritable. I found weak evidence of selection on laying date, associated with both overwinter survival and reproduction in females. The ecological implications of both tarsus length and laying date variation in this population could not be identified. Consequently, although I was able to identify the targets of natural selection, the ecological link between trait variation and selection remains unknown.     

SIZE VARIATION,GROWTH STRATEGIES,AND THE EVOLUTION OF MODULARITY IN THE MAMMALIAN SKULL

Allometry is a major determinant of within‐population patterns of association among traits and, therefore, a major component of morphological integration studies. Even so, the influence of size variation over evolutionary change has been largely unappreciated. Here, we explore the interplay between allometric size variation, modularity, and life‐history strategies in the skull from representatives of 35 mammalian families. We start by removing size variation from within‐species data and analyzing its influence on integration magnitudes, modularity patterns, and responses to selection. We also carry out a simulation in which we artificially alter the influence of size variation in within‐taxa matrices. Finally, we explore the relationship between size variation and different growth strategies. We demonstrate that a large portion of the evolution of modularity in the mammalian skull is associated to the evolution of growth strategies. Lineages with highly altricial neonates have adult variation patterns dominated by size variation, leading to high correlations among traits regardless of any underlying modular process and impacting directly their potential to respond to selection. Greater influence of size variation is associated to larger intermodule correlations, less individualized modules, and less flexible responses to natural selection.     

SEASONAL DECLINES IN OFFSPRING FITNESS AND SELECTION FOR EARLY REPRODUCTION IN NYMPH-OVERWINTERING GRASSHOPPERS

In this study, I examine the effects of natural and experimentally induced variation in life cycle timing on offspring fitness in Arphia sulphurea and Chortophaga viridifasciata, to understand the selective pressures shaping phenology in these two species of nymph-overwintering grasshoppers. Because these species lack embryonic diapause, hatching varies over a two month range under natural conditions. I used a cold treatment to delay hatching of some egg pods and extend the natural range of hatching dates. Due to the shorter time for growth and poorer growing conditions late in the fall, late-hatching nymphs of both species grew to a smaller size before winter and suffered higher overwinter mortality, compared to early nymphs. In addition, late nymphs that did survive the winter became reproductive later in the following year's breeding season. Size- dependent mortality of offspring during the winter is a strong selective pressure favoring early reproduction in these species. Female adult life history traits appear responsive to the seasonal declines in offspring fitness, in that late-maturing females began reproducing sooner after adult maturation and reproduced at a more rapid rate, even at the expense of having shorter adult longevity and producing fewer total egg pods. Experimental manipulations were crucial in understanding the fitness consequences of intrapopulation variation in the timing of specific life-cycle events for these species.     

LABORATORY EVOLUTION OF LIFE-HISTORY TRAITS IN THE BEAN WEEVIL (ACANTHOSCELIDES OBTECTUS): THE EFFECTS OF SELECTION ON DEVELOPMENTAL TIME IN POPULATIONS WITH DIFFERENT PREVIOUS HISTORY

In this study we examined the direct and correlated responses for fast and slow preadult development time in three laboratory populations of the bean weevil (Acanthoscelides obtectus). The first population (“base,” B) has experienced laboratory conditions for more than 10 years; the second (“young,” Y) and the third (“old,” O) populations were selected for early and late reproduction, respectively, before the onset of the present experiments. All three populations are successfully selected for both fast and slow preadult development. The realized heritabilities are very similar in all populations, suggesting a similar level of the additive genetic variance for preadult development. We studied the correlated responses on the following life-history traits: egg-to-adult viability, wet body weight, early fecundity, late fecundity, total realized female fecundity, and adult longevity. All life-history traits examined here, except for the egg-to-adult viability, are affected by selection for preadult development in at least in one of the studied populations. In all three populations, beetles selected for slow preadult development are heavier and live longer than those from the fast-selected lines. The findings with respect to adult longevity are unexpected, because the control Y and O populations, selected for short- and long-lived beetles, respectively, do not show significant differences in preadult development. Thus, our results indicate that some kind of asymmetrical correlated responses occur for preadult development and adult longevity each time that direct selection has been imposed on one or the other of these two traits. In contrast to studies with Drosophila, it appears that for insect species that are aphagous as adults, selection for preadult development entails selection for alleles that also change the adult longevity, but that age-specific selection (applied in the Y and O populations) mostly affects the alleles that have no significant influence on the preadult development. Implications of these findings on the developmental and evolutionary theories of aging are also discussed.     

A TEST AND REVIEW OF THE ROLE OF EFFECTIVE POPULATION SIZE ON EXPERIMENTAL SEXUAL SELECTION PATTERNS

Experimental evolution, particularly experimental sexual selection in which sexual selection strength is manipulated by altering the mating system, is an increasingly popular method for testing evolutionary theory. Concerns have arisen regarding genetic diversity variation across experimental treatments: differences in the number and sex ratio of breeders (effective population size; N_e ) and the potential for genetic hitchhiking, both of which may cause different levels of genetic variation between treatments. Such differences may affect the selection response and confound interpretation of results. Here we use both census-based estimators and molecular marker-based estimates to empirically test how experimental evolution of sexual selection in Drosophila pseudoobscura impacts N_e and autosomal genetic diversity. We also consider effects of treatment on X-linked N_e s, which have previously been ignored. Molecular autosomal marker-based estimators indicate that neither N_e nor genetic diversity differs between treatments experiencing different sexual selection intensities; thus observed evolutionary responses reflect selection rather than any confounding effects of experimental design. Given the increasing number of studies on experimental sexual selection, we also review the census N_e s of other experimental systems, calculate X-linked N_e , and compare how different studies have dealt with the issues of inbreeding, genetic drift, and genetic hitchhiking to help inform future designs.     

MORPHOLOGICAL RATES OF ANGIOSPERM SEED SIZE EVOLUTION

The evolution of seed size among angiosperms reflects their ecological diversification in a complex fitness landscape of life‐history strategies. The lineages that have evolved seeds beyond the upper and lower boundaries that defined nonflowering seed plants since the Paleozoic are more dispersed across the angiosperm phylogeny than would be expected under a neutral model of phenotypic evolution. Morphological rates of seed size evolution estimated for 40 clades based on 17,375 species ranged from 0.001 (Garryales) to 0.207 (Malvales). Comparative phylogenetic analysis indicated that morphological rates are not associated with the clade's seed size but are negatively correlated with the clade's position in the overall distribution of angiosperm seed sizes; clades with seed sizes closer to the angiosperm mean had significantly higher morphological rates than clades with extremely small or extremely large seeds. Likewise, per‐clade taxonomic diversification rates are not associated with the seed size of the clade but with where the clade falls within the angiosperm seed size distribution. These results suggest that evolutionary rates (morphological and taxonomic) are elevated in densely occupied regions of the seed morphospace relative to lineages whose ecophenotypic innovations have moved them toward the edges.     

GENE FLOW AND SELECTION ON PHENOTYPIC PLASTICITY IN AN ISLAND SYSTEM OF RANA TEMPORARIA

Gene flow is often considered to be one of the main factors that constrains local adaptation in a heterogeneous environment. However, gene flow may also lead to the evolution of phenotypic plasticity. We investigated the effect of gene flow on local adaptation and phenotypic plasticity in development time in island populations of the common frog Rana temporaria which breed in pools that differ in drying regimes. This was done by investigating associations between traits (measured in a common garden experiment) and selective factors (pool drying regimes and gene flow from other populations inhabiting different environments) by regression analyses and by comparing pairwise F_ST values (obtained from microsatellite analyses) with pairwise Q_ST values. We found that the degree of phenotypic plasticity was positively correlated with gene flow from other populations inhabiting different environments (among‐island environmental heterogeneity), as well as with local environmental heterogeneity within each population. Furthermore, local adaptation, manifested in the correlation between development time and the degree of pool drying on the islands, appears to have been caused by divergent selection pressures. The local adaptation in development time and phenotypic plasticity is quite remarkable, because the populations are young (less than 300 generations) and substantial gene flow is present among islands.     

ARTIFICIAL SELECTION ON RELATIVE BRAIN SIZE REVEALS A POSITIVE GENETIC CORRELATION BETWEEN BRAIN SIZE AND PROACTIVE PERSONALITY IN THE GUPPY

Animal personalities range from individuals that are shy, cautious, and easily stressed (a “reactive” personality type) to individuals that are bold, innovative, and quick to learn novel tasks, but also prone to routine formation (a “proactive” personality type). Although personality differences should have important consequences for fitness, their underlying mechanisms remain poorly understood. Here, we investigated how genetic variation in brain size affects personality. We put selection lines of large‐ and small‐brained guppies (Poecilia reticulata), with known differences in cognitive ability, through three standard personality assays. First, we found that large‐brained animals were faster to habituate to, and more exploratory in, open field tests. Large‐brained females were also bolder. Second, large‐brained animals excreted less cortisol in a stressful situation (confinement). Third, large‐brained animals were slower to feed from a novel food source, which we interpret as being caused by reduced behavioral flexibility rather than lack of innovation in the large‐brained lines. Overall, the results point toward a more proactive personality type in large‐brained animals. Thus, this study provides the first experimental evidence linking brain size and personality, an interaction that may affect important fitness‐related aspects of ecology such as dispersal and niche exploration.     

INTENSE NATURAL SELECTION ON BODY SIZE AND WING AND TAIL ASYMMETRY IN CLIFF SWALLOWS DURING SEVERE WEATHER

Extreme climatic disturbances provide excellent opportunities to study natural selection in wild populations because they may cause measurable directional shifts in character traits. Insectivorous cliff swallows (Petrochelidon pyrrhonota) in the northern Great Plains must often endure periods of cold weather in late spring that reduce food availability, and if cold spells last four or more days, mortality due to starvation may result. We analyzed morphological shifts associated with viability selection, and how patterns of bilateral symmetry were affected by survival selection, during a four-day period of cold weather in 1992 and a six-day period in 1996 in southwestern Nebraska. Birds that died during the cold were compared to those still alive when the severe weather ended. The event in 1992 killed relatively few birds, but the cold spell in 1996 killed thousands of cliff swallows and reduced their population by about 53%. Climatological records suggest that mortality events comparable to that of 1996 have occurred in only one other year since 1875. Larger birds were favored in the 1996 event. Selection was more intense in 1996 than in 1992 because of more stressful conditions in 1996. Directional selection gradient analysis showed that measures of skeletal body size (tarsus length, culmen width and length) and wing length were targets of selection in 1996. Survivors had lower wing and outer tail asymmetry, and wing and tail asymmetry were targets of selection in both events. Mortality patterns did not differ by sex, but older birds suffered heavier mortality; morphological traits generally did not vary with age. Nonsurvivors were not in poorer apparent condition prior to the weather event than survivors, suggesting that selection acted directly on morphology independent of condition. Selection on body size in cliff swallows was more intense than in studies of body size evolution in other bird species. Larger swallows were probably favored in cold weather due to the thermal advantages of large size and the ability to store more fat. Swallows with low asymmetry were favored probably because low asymmetry in wing and tail made foraging more efficient and less costly, conferring survival advantages during cold weather. This population of cliff swallows may have undergone relatively recent body size evolution.