Density‐dependent offspring interactions do not explain macroevolutionary scaling of adult size and offspring size

Most life forms exhibit a correlated evolution of adult size (AS) and size at independence (SI), giving rise to AS–SI scaling relationships. Theory suggests that scaling arises because relatively large adults have relatively high reproductive output, resulting in strong density‐dependent competition in early life, where large size at independence provides a competitive advantage to juveniles. The primary goal of our study is to test this density hypothesis, using large datasets that span the vertebrate tree of life (fishes, amphibians, reptiles, birds, and mammals). Our secondary goal is to motivate new hypotheses for AS–SI scaling by exploring how subtle variation in life‐histories among closely related species is associated with variation in scaling. Our phylogenetically informed comparisons do not support the density hypothesis. Instead, exploration of AS–SI scaling among life‐history variants suggests that steeper AS–SI scaling slopes are associated with evolutionary increases in size at independence. We suggest that a positive association between size at independence and juvenile growth rate may represent an important mechanism underlying AS–SI scaling, a mechanism that has been underappreciated by theorists. If faster juvenile growth is a consequence of evolutionary increases in size at independence, this may help offset the cost of delayed maturation, leading to steeper AS–SI scaling slopes.     

Mothers produce less aggressive sons with altered immunity when there is a threat of disease during pregnancy

Maternal experience before and during pregnancy is known to play a key role in offspring development. However, the influence of social cues about disease in the maternal environment has not been explored. We indirectly exposed pregnant mice to infected neighbours by housing them next to non-contagious conspecifics infected with Babesia microti. We examined the effect of this indirect immunological exposure on both the females and their adult offspring. Exposed females had higher levels of serum corticosterone and increased kidney growth compared with those with uninfected neighbours. These exposed females subsequently produced offspring that as adults showed an accelerated immune response to B. microti and less aggression in social groups. We suggest that ambient information regarding disease is used adaptively to maximize offspring survival and reproductive success in a challenging environment. Our results shed light on the impact of social information and maternal effects on life histories, and have important consequences for our understanding of epidemiology and individual disease susceptibility in humans and other animals. They also lead us to question the suitability of some laboratory housing conditions during experimental procedures, which may impact negatively upon both animal welfare and the validity of animal science.     

Effect of maternal diet on offspring coping styles in rodents: a systematic review and meta‐analysis

Maternal nutrition can have long‐term effects on offspring morphology, physiology and behaviours. However, it is unclear whether mothers ‘program’ offspring behavioural coping strategy (proactive/reactive) according to the predicted nutritional quality of their future environment. We conducted a systematic review on this topic and meta‐analytically synthesized relevant experimental data on mice and rats (46 studies). We included data from experiments where dams were subjected to caloric restriction, protein restriction or overfeeding around gestation and subsequently measured offspring activity, exploration, or anxiety. Overall, little evidence existed for effects of maternal nutrition on the three investigated behavioural traits. The high heterogeneity observed in the data set suggests that maternal programming may sometimes occur. However, because offspring had access to a balanced diet before testing, behaviours may have been reprogrammed. Our results may indicate that reprogrammed behaviours could ameliorate negative effects associated with sub‐optimal nutrition in early life. Further, our systematic review revealed clear knowledge gaps and fruitful future research avenues.     

Trans‐generational maternal effect: temperature influences egg size of the offspring in Atlantic salmon Salmo salar

Effect of increased temperature during egg maturation on the mass of single eggs produced by the offspring was investigated experimentally in Atlantic salmon Salmo salar. Mass of eggs produced by next‐generation females was larger when their mothers experienced warmer water during the last two months of egg maturation, relative to those that experienced unheated river water. There was no similar trans‐generational paternal effect on offspring egg mass.     

Access to multiple mates increases fecundity but does not affect per‐offspring maternal investment in a marine gastropod

Females of many organisms mate more than once and with more than one male, suggesting that polyandry confers some advantage to the female or her offspring. However, variation in maternal investment in response to mate choice and mate number can confound efforts to determine if there are benefits of polyandry. Access to multiple mates could increase maternal investment in offspring via a number of different mechanisms. Few studies have determined if investment is influenced by mate choice and number, and data are particularly lacking for marine invertebrates. This study was designed to determine if maternal investment and offspring size increase with access to increasing numbers of mates in the protandrous intertidal slipper snail Crepidula cf. marginalis. Virgin female slipper limpets were exposed to one, three, or five potential mates and their fecundity, egg size, and hatchling size were measured for multiple clutches. Treatment had a significant effect on fecundity, with fecundity increasing with the number of potential mates. Treatment did not have an effect on the size of eggs or hatchlings, on the variation in egg size or hatchling size within broods, or on the frequency of oviposition. Treatment did alter the variation in average offspring size among females, but not in the way predicted by theory. The main result, that access to multiple mates does not have an effect on per offspring maternal investment, makes C. cf. marginalis an ideal candidate to study the effects of polyandry on offspring fitness without having to take into account confounding effects of variation in maternal investment.     

Maternal sexual interactions affect offspring survival and ageing

In many species, females exposed to increased sexual activity experience reductions in longevity. Here, in Drosophila melanogaster, we report an additional effect on females brought about by sexual interactions, an effect that spans generations. We subjected females to a sexual treatment consisting of different levels of sexual activity and then investigated patterns of mortality in their offspring. We found reduced probabilities of survival, increases in the rate of senescence and a pattern of reduced mean longevities, for offspring produced by mothers that experienced higher levels of sexual interaction. We contend that these effects constitute trans‐generational costs of sexual conflict – the existence or implications of which have rarely been considered previously. Our results indicate that ongoing exposure by mothers to male precopulatory interactions is itself sufficient to drive trans‐generational effects on offspring mortality. Thus, we show that increases in maternal sexual activity can produce trans‐generational effects that permeate through to latter life stages in the offspring. This helps to elucidate the complex interplay between sex and ageing and provides new insights into the dynamics of adaptation under sexual selection.     

Intergenerational effects of maternal birth season on offspring size in rural Gambia

Environmental conditions experienced in early life can influence an individual's growth and long-term health, and potentially also that of their offspring. However, such developmental effects on intergenerational outcomes have rarely been studied. Here we investigate intergenerational effects of early environment in humans using survey- and clinic-based data from rural Gambia, a population experiencing substantial seasonal stress that influences foetal growth and has long-term effects on first-generation survival. Using Fourier regression to model seasonality, we test whether (i) parental birth season has intergenerational consequences for offspring in utero growth (1982 neonates, born 1976-2009) and (ii) whether such effects have been reduced by improvements to population health in recent decades. Contrary to our predictions, we show effects of maternal birth season on offspring birth weight and head circumference only in recent maternal cohorts born after 1975. Offspring birth weight varied according to maternal birth season from 2.85 to 3.03 kg among women born during 1975-1984 and from 2.84 to 3.41 kg among those born after 1984, but the seasonality effect reversed between these cohorts. These results were not mediated by differences in maternal age or parity. Equivalent patterns were observed for offspring head circumference (statistically significant) and length (not significant), but not for ponderal index. No relationships were found between paternal birth season and offspring neonatal anthropometrics. Our results indicate that even in rural populations living under conditions of relative affluence, brief variation in environmental conditions during maternal early life may exert long-term intergenerational effects on offspring.     

Length of intervals between epidemics: evaluating the influence of maternal transfer of immunity

The length of intervals between epidemic outbreaks of infectious diseases is critical in epidemiology. In several species of marine mammals and birds, it is pivotal to also consider the life history of the species of concern, as the contact rate between individuals can have a seasonal flux, for example, due to aggregations during the breeding season. Recently, particular interest has been given to the role of the dynamics of immunity in determining the intervals between epidemics in wild animal populations. One potentially powerful, but often neglected, process in this context is the maternal transfer of immunity. Here, we explore theoretically how the transfer of maternal antibodies can delay the recurrence of epidemics using Phocine Distemper in harbor seals as an example of a system in which epidemic outbreaks are followed by pathogen extinction. We show that the presence of temporarily protected newborns can significantly increase the predicted interval between epidemics, and this effect is strongly dependent on the degree of synchrony in the breeding season. Furthermore, we found that stochasticity in the onset of epidemics in combination with maternally acquired immunity increases the predicted intervals between epidemics even more. These effects arise because newborns with maternal antibodies temporarily boost population level immunity above the threshold of herd immunity, particularly when breeding is synchronous. Overall, our results show that maternal antibodies can have a profound influence on the dynamics of wildlife epidemics, notably in gregarious species such as many marine mammals and seabirds.     

Bigger is better: age class-specific survival rates in long-lived turtles increase with size

Vital rates for small, non-breeding individuals are important components of population dynamics for many species, but often individuals of these sizes are difficult to locate, capture, and track. As such, biologists frequently lack reliable estimates of juvenile survival because sample sizes and recapture rates for this life stage are low. Long-lived animals often take many years to reach sexual maturity and spend much of this time in the smaller size classes, making them sensitive to changes in survival rates. We estimated the survival rates of all size classes for the northern map turtle (Graptemys geographica) using a mark-recapture dataset with >3,500 captures from 2019–2021 and 210 nests from 2018–2021. As turtle size increased, annual survival probability increased regardless of sex. Estimated annual survival probability for turtles >18 cm long (i.e., adult females >15 years) was about 0.95, over 4 times higher than turtles that were 3 cm long (i.e., hatchlings <1 year; 0.22 annual survival probability). Although we did not observe a difference in survival probability between sexes of any size class, adult females are nearly twice the size of adult males, leading to an increased annual survival probability for females of 0.95, compared to 0.80 for males. Changes in adult survival had the greatest influence on population estimates over time, with temporary decreases, such as those due to poaching or an environmental disaster, potentially leading to unrecoverable decreases in the overall population size. Our study provides detailed survival rates for all size classes in a long-lived turtle, which are necessary to assess population stability and can be used to determine the most effective conservation or management practices.     

The adaptive significance of population differentiation in offspring size of the least killifish,Heterandria formosa

We tested the hypothesis that density‐dependent competition influences the evolution of offspring size. We studied two populations of the least killifish (Heterandria formosa) that differ dramatically in population density; these populations are genetically differentiated for offspring size, and females from both populations produce larger offspring when they experience higher social densities. To look at the influences of population of origin and relative body size on competitive ability, we held females from the high‐density population at two different densities to create large and small offspring with the same genetic background. We measured the competitive ability of those offspring in mesocosms that contained either pure or mixed population treatments at either high or low density. High density increased competition, which was most evident in greatly reduced individual growth rates. Larger offspring from the high‐density population significantly delayed the onset of maturity of fish from the low‐density population. From our results, we infer that competitive conditions in nature have contributed to the evolution of genetically based interpopulation differences in offspring size as well as plasticity in offspring size in response to conspecific density.     

No effect of host–parasite co‐evolution on host range expansion

Antagonistic co‐evolution between hosts and parasites (reciprocal selection for resistance and infectivity) is hypothesized to play an important role in host range expansion by selecting for novel infectivity alleles, but tests are lacking. Here, we determine whether experimental co‐evolution between a bacterium (Pseudomonas fluorescens SBW25) and a phage (SBW25Φ2) affects interstrain host range: the ability to infect different strains of P. fluorescens other than SBW25. We identified and tested a genetically and phenotypically diverse suite of co‐evolved phage variants of SBW25Φ2 against both sympatric and allopatric co‐evolving hosts (P. fluorescens SBW25) and a large set of other P. fluorescens strains. Although all co‐evolved phage had a greater host range than the ancestral phage and could differentially infect co‐evolved variants of P. fluorescens SBW25, none could infect any of the alternative P. fluorescens strains. Thus, parasite generalism at one genetic scale does not appear to affect generalism at other scales, suggesting fundamental genetic constraints on parasite adaptation for this virus.     

Assessment of correlational selection on tolerance and resistance traits in a host plant–parasitic plant interaction

Resistance and tolerance are considered to be different plant strategies against disease. While resistance traits prevent hosts becoming parasitized or reduce the extent of parasitism, tolerance traits reduce the fitness-impact of parasitism on infected hosts. Theoretical considerations predict that in some circumstances mutual redundancy will give hosts with either high resistance or high tolerance a fitness advantage over hosts that exhibit both of these traits together. However, empirical evidence has provided mixed results. In this paper, I describe the pattern of phenotypic selection imposed by the holoparasitic mistletoe Tristerix aphyllus upon resistance (spine length) and tolerance (branching) traits in the cactus Echinopsis chilensis. Results indicate that branching was an efficient compensatory mechanism, reducing 75.5% of the fitness-impact attributable to parasitism. Even though both traits showed a negative correlation, as expected from the presence of allocation costs between strategies, no correlational selection coefficient was significant indicating that selection did not favor alternative combinations of traits. Consequently, I did not find evidence for selection promoting mutually exclusive defense strategies against the mistletoe, which suggests that tolerance and resistance traits may coexist stably in populations of E. chilensis.     

Host‐parasite coevolution can promote the evolution of seed banking as a bet‐hedging strategy

Seed (egg) banking is a common bet‐hedging strategy maximizing the fitness of organisms facing environmental unpredictability by the delayed emergence of offspring. Yet, this condition often requires fast and drastic stochastic shifts between good and bad years. We hypothesize that the host seed banking strategy can evolve in response to coevolution with parasites because the coevolutionary cycles promote a gradually changing environment over longer times than seed persistence. We study the evolution of host germination fraction as a quantitative trait using both pairwise competition and multiple mutant competition methods, while the germination locus can be genetically linked or unlinked with the host locus under coevolution. In a gene‐for‐gene model of coevolution, hosts evolve a seed bank strategy under unstable coevolutionary cycles promoted by moderate to high costs of resistance or strong disease severity. Moreover, when assuming genetic linkage between coevolving and germination loci, the resistant genotype always evolves seed banking in contrast to susceptible hosts. Under a matching‐allele interaction, both hosts’ genotypes exhibit the same seed banking strategy irrespective of the genetic linkage between loci. We suggest host–parasite coevolution as an additional hypothesis for the evolution of seed banking as a temporal bet‐hedging strategy.     

Age‐dependent effects of predation risk on reproductive success in a freshwater snail

Reproductive performance is often age‐dependent, showing patterns of improvement and/or senescence as well as trade‐offs with other traits throughout the lifespan. High levels of extrinsic mortality (e.g., from predators) have been shown to sometimes, but not always, select for accelerated actuarial senescence in nature and in the lab. Here, we explore the inductive (i.e., plastic) effects of predation risk (i.e., nonlethal exposure to chemical cues from predators) on the reproductive success of freshwater snails (Physa acuta). Snails were reared either in the presence or absence of chemical cues from predatory crayfish and mated early in life or late in life (a 2 × 2 factorial design); we measured egg hatching and early post‐hatching survival of their offspring. Both age and predation risk reduced reproductive success, illustrating that predation risk can have a cross‐generational effect on the early survival of juveniles. Further, the decline in reproductive success was over three times faster under predation risk compared to the no‐predator treatment, an effect that stemmed from a disproportionate, negative effect of predation risk on the post‐hatching survival instead of hatching rate. We discuss our results in terms of a hypothesized consequence of elevated stress hormone levels.     

Maternal effects on offspring size in a natural population of the viviparous tsetse fly

1. Theory predicts that mothers should adaptively adjust reproductive investment depending on current reserves and future reproductive opportunities. Females in better intrinsic state, or with more resources, should invest more in current reproduction than those with fewer resources. Across the lifespan, investment may increase as future reproductive opportunities decline, yet may also decline with reductions in intrinsic state. 2. Across many species, larger mothers produce larger offspring, but there is no theoretical consensus on why this is so. This pattern may be driven by variation in maternal state such as nutrition, yet few studies measure both size and nutritional state or attempt to tease apart confounding effects of size and age. 3. Viviparous tsetse flies (Glossina species) offer an excellent system to explore patterns of reproductive investment: females produce large, single offspring sequentially over the course of their relatively long life. Thus, per‐brood reproductive effort can be quantified by offspring size. 4. While most tsetse reproduction research has been conducted on laboratory colonies, maternal investment was investigated in this study using a unique field method where mothers were collected as they deposited larvae, allowing simultaneous mother‐offspring measurements under natural conditions. 5. It was found that larger mothers and those with a higher fat content produced larger offspring, and there was a trend for older mothers to produce slightly larger offspring. 6. The present results highlight the importance of measuring maternal nutritional state, rather than size alone, when considering maternal investment in offspring. Implications for understanding vector population dynamics are also discussed.