When bigger is not better: selection against large size, high condition and fast growth in juvenile lemon sharks

Selection acting on large marine vertebrates may be qualitatively different from that acting on terrestrial or freshwater organisms, but logistical constraints have thus far precluded selection estimates for the former. We overcame these constraints by exhaustively sampling and repeatedly recapturing individuals in six cohorts of juvenile lemon sharks (450 age-0 and 255 age-1 fish) at an enclosed nursery site (Bimini, Bahamas). Data on individual size, condition factor, growth rate and inter-annual survival were used to test the 'bigger is better', 'fatter is better' and 'faster is better' hypotheses of life-history theory. For age-0 sharks, selection on all measured traits was weak, and generally acted against large size and high condition. For age-1 sharks, selection was much stronger, and consistently acted against large size and fast growth. These results suggest that selective pressures at Bimini may be constraining the evolution of large size and fast growth, an observation that fits well with the observed small size and low growth rate of juveniles at this site. Our results support those of some other recent studies in suggesting that bigger/fatter/faster is not always better, and may often be worse.     

A genetic assessment of polyandry and breeding-site fidelity in lemon sharks

We here employ 11 microsatellite markers and recently developed litter reconstruction methods to infer mating system parameters (i.e. polyandry and breeding-site fidelity) at a lemon shark nursery site in Marquesas Key, Florida. Four hundred and eight juvenile or subadult sharks were genotyped over eight complete breeding seasons. Using this information, we were able to infer family structure, as well as fully or partially reconstruct genotypes of 46 mothers and 163 fathers. Multiple litter reconstruction methods were used, and novel simulations helped define apparent bias and precision of at least some mating system parameters. For Marquesas Key, we find that adult female lemon sharks display high levels of polyandry (81% of all litters sampled) and stronger fidelity to the nursery site than do males. Indeed, few male sharks sired offspring from more than one litter during the course of the study. These findings were quite similar to previous results from another lemon shark nursery site (Bimini, Bahamas), suggesting conserved mating system parameters despite significant variation in early life-history traits (i.e. body size and growth) among sites. The finding of at least some site fidelity in females also supports the need for careful conservation of each nursery.     

Are indirect genetic benefits associated with polyandry? Testing predictions in a natural population of lemon sharks

Multiple mating has clear fitness benefits for males, but uncertain benefits and costs for females. We tested for indirect genetic benefits of polyandry in a natural population, by using data from a long-term genetic and demographic study of lemon sharks ( Negaprion brevirostris ) at Bimini, Bahamas. To do so, we followed the fates of individuals from six cohorts (450 age-0 and 254 age-1 fish) in relation to their individual level of genetic variation, and whether they were from polyandrous or monoandrous litters. We find that offspring from polyandrous litters did not have a greater genetic diversity or greater survival than did the offspring of monoandrous litters. We also find no evidence of positive associations between individual offspring genetic diversity metrics and our surrogate measure of fitness (i.e. survival). In fact, age-1 individuals with fewer heterozygous microsatellite loci and more genetically similar parents were more likely to survive to age-2. Thus, polyandry in female lemon sharks does not appear to be adaptive from the perspective of indirect genetic benefits to offspring. It may instead be the result of convenience polyandry, whereby females mate multiply to avoid harassment by males. Our inability to find indirect genetic benefits of polyandry despite detailed pedigree and survival information suggests the need for similar assessments in other natural populations.     

Novel Acoustic Technology for Studying Free-Ranging Shark Social Behaviour by Recording Individuals' Interactions

Group behaviours are widespread among fish but comparatively little is known about the interactions between free-ranging individuals and how these might change across different spatio-temporal scales. This is largely due to the difficulty of observing wild fish groups directly underwater over long enough time periods to quantify group structure and individual associations. Here we describe the use of a novel technology, an animal-borne acoustic proximity receiver that records close-spatial associations between free-ranging fish by detection of acoustic signals emitted from transmitters on other individuals. Validation trials, held within enclosures in the natural environment, on juvenile lemon sharks Negaprion brevirostris fitted with external receivers and transmitters, showed receivers logged interactions between individuals regularly when sharks were within 4 m (∼4 body lengths) of each other, but rarely when at 10 m distance. A field trial lasting 17 days with 5 juvenile lemon sharks implanted with proximity receivers showed one receiver successfully recorded association data, demonstrating this shark associated with 9 other juvenile lemon sharks on 128 occasions. This study describes the use of acoustic underwater proximity receivers to quantify interactions among wild sharks, setting the scene for new advances in understanding the social behaviours of marine animals.     

Estimating quantitative genetic parameters in wild populations: a comparison of pedigree and genomic approaches

The estimation of quantitative genetic parameters in wild populations is generally limited by the accuracy and completeness of the available pedigree information. Using relatedness at genomewide markers can potentially remove this limitation and lead to less biased and more precise estimates. We estimated heritability, maternal genetic effects and genetic correlations for body size traits in an unmanaged long‐term study population of Soay sheep on St Kilda using three increasingly complete and accurate estimates of relatedness: (i) Pedigree 1, using observation‐derived maternal links and microsatellite‐derived paternal links; (ii) Pedigree 2, using SNP‐derived assignment of both maternity and paternity; and (iii) whole‐genome relatedness at 37 037 autosomal SNPs. In initial analyses, heritability estimates were strikingly similar for all three methods, while standard errors were systematically lower in analyses based on Pedigree 2 and genomic relatedness. Genetic correlations were generally strong, differed little between the three estimates of relatedness and the standard errors declined only very slightly with improved relatedness information. When partitioning maternal effects into separate genetic and environmental components, maternal genetic effects found in juvenile traits increased substantially across the three relatedness estimates. Heritability declined compared to parallel models where only a maternal environment effect was fitted, suggesting that maternal genetic effects are confounded with direct genetic effects and that more accurate estimates of relatedness were better able to separate maternal genetic effects from direct genetic effects. We found that the heritability captured by SNP markers asymptoted at about half the SNPs available, suggesting that denser marker panels are not necessarily required for precise and unbiased heritability estimates. Finally, we present guidelines for the use of genomic relatedness in future quantitative genetics studies in natural populations.     

A general model for the scaling of offspring size and adult size

Understanding evolutionary coordination among different life-history traits is a key challenge for ecology and evolution. Here we develop a general quantitative model predicting how offspring size should scale with adult size by combining a simple model for life-history evolution with a frequency-dependent survivorship model. The key innovation is that larger offspring are afforded three different advantages during ontogeny: higher survivorship per time, a shortened juvenile phase, and advantage during size-competitive growth. In this model, it turns out that size-asymmetric advantage during competition is the factor driving evolution toward larger offspring sizes. For simplified and limiting cases, the model is shown to produce the same predictions as the previously existing theory on which it is founded. The explicit treatment of different survival advantages has biologically important new effects, mainly through an interaction between total maternal investment in reproduction and the duration of competitive growth. This goes on to explain alternative allometries between log offspring size and log adult size, as observed in mammals (slope = 0.95) and plants (slope = 0.54). Further, it suggests how these differences relate quantitatively to specific biological processes during recruitment. In these ways, the model generalizes across previous theory and provides explanations for some differences between major taxa.     

Heterochrony and the evolution of poecilogony: generating larval diversity

Poecilogony is the production of more than one type of young within a single species of marine invertebrate. We chose a poecilogonous polychaete to investigate potential differences in morphogenesis among offspring that are polymorphic in dispersal potentials (planktonic, benthic) and trophic modes (planktotrophy, adelphophagy). Differences in morphogenesis occur and are strongly influenced by maternal type. Females that provide extra-embryonic nutrition (as nurse eggs; type III females) also produce offspring with an accelerated onset of juvenile traits, relative to planktotrophic offspring of females that do not provide extra-embryonic nutrition (type I females). Thus, progeny of some females appear morphologically preadapted for a benthic lifestyle. Surprisingly, differences in phenotype among offspring do not parallel offspring ecotype, as offspring with early onset of juvenile traits (III) are ecologically bimodal. Some Type III offspring eat the nurse eggs (adelphophagy), have accelerated development, and hatch as benthic juveniles. In contrast, their siblings hatch as small, planktotrophic, dispersive larvae that are morphologically similar to their type III siblings, but ecologically similar to Type I planktotrophic larvae. We propose that poecilogony evolved through sequence heterochrony in morphogenesis with accelerated onset of juvenile traits in type III offspring. In addition, we suggest that heterochrony in life-history events (hatching, metamorphosis) also occurs, thereby generating offspring that are dimorphic in both phenotype and ecotype. Over time, selection acting on different levels of ontogeny (morphogenesis vs. dispersal) may balance this polymorphism and allow poecilogony to persist.     

Hybridization and invasiveness in the freshwater snail Melanoides tuberculata: hybrid vigour is more important than increase in genetic variance

Many invasive taxa are hybrids, but how hybridization boosts the invasive process remains poorly known. We address this question in the clonal freshwater snail Melanoides tuberculata from Martinique, using three parental and two hybrid lines. We combine an extensive field survey (1990-2003) and a quantitative genetic experiment to show that hybrid lines have outcompeted their parents in natural habitats, and that this increased invasiveness co-occurred with pronounced shifts in life-history traits, such as growth, fecundity and juvenile size. Given the little time between hybrid creation and sampling, and the moderate standing genetic variance for life-history traits in hybrids, we show that some of the observed trait changes between parents and hybrids were unlikely to arise only by continuous selection. We therefore suggest that a large part of hybrid advantage stems from immediate heterosis upon hybridization.     

The population determines whether and how life-history traits vary between reproductive events in an insect with maternal care

The last reproductive event of a female is often associated with major changes in terms of both maternal and offspring life-history traits. However, the nature of these changes and the importance of population-specific environmental constraints in shaping their expression are difficult to predict and, as a consequence, poorly understood. Here, we investigated whether and how life-history traits vary between reproductive events and whether this variation is population-dependent in the European earwig Forficula auricularia. In this insect species, females produce up to two clutches during their lifetime and express extensive forms of maternal care. We conducted a common garden experiment, in which we measured 11 life-history traits of the first and second clutches of 132 females originating from three populations. Our results showed that clutch size was higher and the level of care expressed towards juveniles lower in second as compared to the first clutches in all three populations. In contrast, we found a population-specific effect on whether and how the reproductive event shaped juvenile quality and a trade-off between egg developmental time and female weight at hatching. Overall, these findings emphasise that the last reproductive event of a female entails both positive and negative effects on various life-history traits of the female herself and her clutch of juveniles. Moreover, our study stresses the importance of population idiosyncrasies on the expression and nature of such cohort-specific effects.     

Interpopulation variation in life-history traits of Poeciliopsis prolifica: implications for the study of placental evolution

Placental reproduction is widespread across vertebrate taxa, but little is known about its life-history correlates and putative adaptive value. We studied variation in life-history traits in two populations of the placental poeciliid fish Poeciliopsis prolifica to determine whether differences in post-fertilization maternal provisioning to embryos have a genetic basis and how food availability affects reproduction. Life histories were characterized for wild-caught females and for second-generation lab-born females raised under two levels of food availability. We found that the two populations did not differ significantly in the wild for any life-history traits except for the lipid dry weight in females and in embryos at an advanced stage of development. When environmental effects were experimentally controlled, however, populations exhibited significant differences in several traits, including the degree of maternal provisioning to embryos. Food availability significantly affected female size at first parturition, brood size and offspring dry weight at birth. Altogether, these results demonstrate that population differences in maternal provisioning and other life-history traits have a genetic basis and show a plastic response to food availability. We infer that phenotypic plasticity may mask population differences in the field. In addition, when comparing life-history patterns in these two populations with known patterns in placental and non-placental poeciliids, our results support the hypotheses that placentation is an adaptive reproductive strategy under high-resource conditions but that it may represent a cost under low-food conditions. Finally, our results highlight that age at maturity and reproductive allotment may be key life-history traits accompanying placental evolution.     

Homing ability of young lemon sharks, <Emphasis Type="Italic">Negaprion brevirostris</Emphasis>

Synopsis We carried out the first experimental study testing an elasmobranchs ability to return home. We displaced juvenile lemon sharks,Negaprion brevirostris, 4–16 km from their observed home ranges at Bimini Islands, Bahamas during daylight and at night. We tracked all sharks except one back to the Bimini Islands and most returned to their home ranges observed before displacement. Even sharks displaced to a site closer to another island with suitable habitat for young lemon sharks returned to their home ranges at Bimini Islands. Sharks displayed a preferred compass direction (PCD) toward the east as their first swimming direction after release, suggesting an innate sense of direction. This bearing was followed shortly afterwards by a home-oriented direction. Swimming speeds prior to reaching shore were approximately twice as fast than the usual cruising speed reported for juvenile lemon sharks. The return of young (0–2 years), inexperienced sharks to their original home range indicate high site fidelity and an ability to home.     

Effects of spontaneous mutation accumulation on sex ratio traits in a parasitoid wasp

Sex allocation theory has proved extremely successful at predicting when individuals should adjust the sex of their offspring in response to environmental conditions. However, we know rather little about the underlying genetics of sex ratio or how genetic architecture might constrain adaptive sex-ratio behavior. We examined how mutation influenced genetic variation in the sex ratios produced by the parasitoid wasp Nasonia vitripennis. In a mutation accumulation experiment, we determined the mutability of sex ratio, and compared this with the amount of genetic variation observed in natural populations. We found that the mutability (h(2)(m)) ranges from 0.001 to 0.002, similar to estimates for life-history traits in other organisms. These estimates suggest one mutation every 5-60 generations, which shift the sex ratio by approximately 0.01 (proportion males). In this and other studies, the genetic variation in N. vitripennis sex ratio ranged from 0.02 to 0.17 (broad-sense heritability, H(2)). If sex ratio is maintained by mutation-selection balance, a higher genetic variance would be expected given our mutational parameters. Instead, the observed genetic variance perhaps suggests additional selection against sex-ratio mutations with deleterious effects on other fitness traits as well as sex ratio (i.e., pleiotropy), as has been argued to be the case more generally.     

Living fast and dying young: A comparative analysis of life-history variation among mammals

Recent comparative studies point to the importance of mortality schedules as determinants in the evolution of life-history characteristics. In this paper, we compare patterns of mortality from natural populations of mammals with a variety of life histories. We find that, after removing the effects of body weight, mortality is the best predictor of variation in life-history traits. Mammals with high levels of natural mortality tend to mature early and give birth to small offspring in large litters after a short gestation, before and after body size effects are factored out. We examine the way in which life-history traits relate to juvenile mortality versus adult mortality and find that juvenile mortality is more highly correlated with life-history traits than is adult mortality. We discuss the necessity of distinguishing between extrinsic sources of mortality (e.g. predation) and mortality caused by intrinsic sources (e.g. costs of reproduction), and the role that ecology might play in the evolution of patterns of mortality and fecundity. We conclude that these results must be explained not simply in the light of the demographic necessity of balancing mortality and fecundity, but as a result of age-specific costs and benefits of reproduction and parental investment. Detailed comparative studies of mortality patterns in natural populations of mammals offer a promising avenue towards understanding the evolution of life-history strategies.     

Sources of genetic and phenotypic variance in fertilization rates and larval traits in a sea urchin

In nonresource based mating systems females are thought to derive indirect genetic benefits by mating with high-quality males. Such benefits can be due either to the intrinsic genetic quality of sires or to beneficial interactions between maternal and paternal haplotypes. Animals with external fertilization and no parental care offer unrivaled opportunities to address these hypotheses. With these systems, cross-classified breeding designs and in vitro fertilization can be used to disentangle sources of genetic and environmental variance in offspring fitness. Here, we employ these approaches in the Australian sea urchin Heliocidaris erythrogramma and explore how sire-dam identities influence fertilization rates, embryo viability (survival to hatching), and metamorphosis, as well as the interrelationships between these potential fitness traits. We show that fertilization is influenced by a combination of strong maternal effects and intrinsic male effects. Our subsequent analysis of embryo viability, however, revealed a highly significant interaction between parental genotypes, indicating that partial incompatibilities can severely limit offspring survival at this life-history stage. Importantly, we detected no significant relationship between fertilization rates and embryo viability. This finding suggests that fertilization rates should not be inferred from hatching rates, which is commonly practiced in species in which it is not possible to estimate fertilization at conception. Finally, we detected significant additive genetic variance due to sires in rates of juvenile metamorphosis, and a positive correlation between fertilization rates and metamorphosis. This latter finding indicates that the performance of a male's ejaculate in noncompetitive IVF trials predicts heritable offspring traits, although the fitness implications of variance in rates of spontaneous juvenile metamorphosis have yet to be determined.     

The role of maternal effects on offspring performance in familiar and novel environments

Maternal effects are an important evolutionary force that may either facilitate adaptation to a new environment or buffer against unfavourable conditions. The degree of variation in traits expressed by siblings from different mothers is often sensitive to environmental conditions. This could generate a Maternal-by-Environment interaction (M × E) that inflates estimates of Genotype-by-Environment effects (G × E). We aimed to test for environment-specific maternal effects (M × E) using a paternal full-sib/half-sib breeding design in the seed beetle Callosobruchus maculatus, where we split and reared offspring from the same mother on two different bean host types—original and novel. Our quantitative genetic analysis indicated that maternal effects were very small on both host types for all the measured life-history traits. There was also little evidence that maternal oviposition preference for a particular host type predicted her offspring’s performance on that host. Further, additive genetic variance for most traits was relatively high on both hosts. While there was higher heritability for offspring reared in the novel host, there was no evidence for G × Es, and most cross-host genetic correlations were positive. This suggests that offspring from the same family ranked similarly for performance on both host types. Our results point to a genetic basis of host adaptation in the seed beetle, rather than maternal effects. Even so, we encourage researchers to test for potential M × Es because, due to a lack of testing, it remains unclear how often they arise.Subject terms: Evolutionary genetics, Quantitative trait     

GENETIC AND ENVIRONMENTAL VARIATION IN LIFE-HISTORY TRAITS OF A MONOCARPIC PERENNIAL: A DECADE-LONG FIELD EXPERIMENT

Directional and stabilizing selection tend to deplete additive genetic variance. On the other hand, genetic variance in traits related to fitness could be retained through polygenic mutation, spatially varying selection, genotype-environment interaction, or antagonistic pleiotropy. Most estimates of genetic variance in fitness-related traits have come from laboratory studies, with few estimates of heritability made under natural conditions, particularly for longer lived organisms. Here I estimated additive genetic variance in life-history characters of a monocarpic herb, Ipomopsis aggregata, that lives for up to a decade. Experimental crosses yielded 229 full-sibships nested within 32 paternal half-sibships. More than 5000 offspring were planted as seeds into natural field sites and were followed in most cases through their entire life cycle. Survival showed substantial additive genetic variance (genetic coefficient of variation ≈ 54%). Small differences at seedling emergence were magnified over time, such that the genetic variability in survival was only detectable by tracking the success of offspring for several years starting from seed. In contrast to survival, reproductive traits such as flower number, seeds per flower, and age at flowering showed little or no genetic variability. Despite relatively high levels of additive genetic variation for some life-history characters, high environmental variance in survival resulted in very low heritabilities (0–9%) for all of these characters. Maternal effects were evident in seed mass and remained strong throughout the lengthy vegetative period. No negative genetic correlations between major components of female fitness were detected. Mean corolla width for a paternal family was, however, negatively correlated with the finite rate of increase based on female fitness. That negative correlation could help to maintain additive genetic variance in the face of strong selection through male function for wide corollas.     

Fitness drivers in the threatened Dianthus guliae Janka (Caryophyllaceae): disentangling effects of growth context, maternal influence and inbreeding depression

We studied inbreeding depression, growth context and maternal influence as constraints to fitness in the self-compatible, protandrous Dianthus guliae Janka, a threatened Italian endemic. We performed hand-pollinations to verify outcomes of self- and cross-fertilisation over two generations, and grew inbred and outbred D.?guliae offspring under different conditions - in pots, a common garden and field conditions (with/without nutrient addition). The environment influenced juvenile growth and flowering likelihood/rate, but had little effect on inbreeding depression. Significant interactions among genetic and environmental factors influenced female fertility. Overall, genetic factors strongly affected both early (seed mass, seed germination, early survival) and late (seed/ovule ratio) life-history traits. After the first pollination experiment, we detected higher mortality in the selfed progeny, which is possibly a consequence of inbreeding depression caused by over-expression of early-acting deleterious alleles. The second pollination induced a strong loss of reproductive fitness (seed production, seed mass) in inbred D.?guliae offspring, regardless of the pollination treatment (selfing/crossing); hence, a strong (genetic) maternal influence constrained early life-history traits of the second generation. Based on current knowledge, we conclude that self-compatibility does not prevent the detrimental effects of inbreeding in D.?guliae populations, and may increase the severe extinction risk if out-crossing rates decrease.     

Spatial ecology of juvenile lemon sharks (<Emphasis Type="Italic">Negaprion brevirostris</Emphasis>) in tidal creeks and coastal waters of Eleuthera,The Bahamas

Fisheries exploitation and habitat alteration are threatening lemon shark (Negaprion bevirostris) populations because they use nearshore regions as nursery sites. As such, there is a need for information on the spatial ecology of juvenile lemon sharks to identify critical habitats that require protection, as well as to understand their basic ecology. The purpose of this study was to determine the habitat preferences and movement patterns of juvenile lemon sharks along a sub-section of coastline characterized by coastal flats and tidal creeks of Eleuthera, The Bahamas. Eleven juvenile lemon sharks (766 ± 127 mm total length; mean±SD) were captured from various tidal creeks within the 23 km study area and were surgically implanted with acoustic transmitters. A series of 27 hydrophone receivers acted as a passive monitoring array to detect tagged individuals as they moved among habitats. Findings suggest that juvenile lemon sharks tagged in this study prefer shallow water habitats within tidal creeks, and typically display high site fidelity with occasional forays to alternate habitats or creeks. In fact, more than 90% of tagged lemon sharks had the greatest percentage of detections located at a receiver at or close to the location where they were tagged. There was no evidence of differences in diel or seasonal movement and habitat use. Knowledge gained from this study will be useful for directing future conservation and management strategies including coastal development plans and marine protected areas.     

Spatial and ontogenetic variation in growth of nursery-bound juvenile lemon sharks, <Emphasis Type="Italic">Negaprion brevirostris</Emphasis>: a comparison of two age-assigning techniques

Synopsis We compared growth rates of the lemon shark, Negaprion brevirostris, from Bimini, Bahamas and the Marquesas Keys (MK), Florida using data obtained in a multi-year annual census. We marked new neonate and juvenile sharks with unique electronic identity tags in Bimini and in the MK we tagged neonate and juvenile sharks. Sharks were tagged with tiny, subcutaneous transponders, a type of tagging thought to cause little, if any disruption to normal growth patterns when compared to conventional external tagging. Within the first 2 years of this project, no age data were recorded for sharks caught for the first time in Bimini. Therefore, we applied and tested two methods of age analysis: (1) a modified minimum convex polygon method and (2) a new age-assigning method, the cut-off technique. The cut-off technique proved to be the more suitable one, enabling us to identify the age of 134 of the 642 previously unknown aged sharks. This maximised the usable growth data included in our analysis. Annual absolute growth rates of juvenile, nursery-bound lemon sharks were almost constant for the two Bimini nurseries and can be best described by a simple linear model (growth data was only available for age-0 sharks in the MK). Annual absolute growth for age-0 sharks was much greater in the MK than in either the North Sound (NS) and Shark Land (SL) at Bimini. Growth of SL sharks was significantly faster during the first 2 years of life than of the sharks in the NS population. However, in MK, only growth in the first year was considered to be reliably estimated due to low recapture rates. Analyses indicated no significant differences in growth rates between males and females for any area.This revised version was published online in April 2005 with corrections to the fourth authors email address and affiliation.     

First summer growth predetermined in anadromous and resident brook charr

Early growth of wild, anadromous and non-anadromous (resident) brook charr Salvelinus fontinalis was compared under controlled laboratory conditions. Offspring were collected as they emerged from natural redds in the Miramichi River, New Brunswick, Canada. Anadromous offspring were initially longer and heavier than residents. Anadromous offspring had lower specific growth rates during their first 2 months post-emergence, but surpassed residents by the third month. Consequently, anadromous offspring remained larger at the end of 3 months and it is concluded that they had a predetermined, maternal and genetic advantage related to body size, rather than an environmentally determined advantage during their first summer of growth. Other studies hypothesize that juvenile development affects life-history strategy adopted as adults, which suggests anadromy in this population may be, at least in part, predetermined by maternal and genetic effects.