Faster is not always better: selection on growth rate fluctuates across life history and environments

Growth rate is increasingly recognized as a key life-history trait that may affect fitness directly rather than evolve as a by-product of selection on size or age. An ongoing challenge is to explain the abundant levels of phenotypic and genetic variation in growth rates often seen in natural populations, despite what is expected to be consistently strong selection on this trait. Such a paradox suggests limits to how contemporary growth rates evolve. We explored limits arising from variation in selection, based on selection differentials for age-specific growth rates expressed under different ecological conditions. We present results from a field experiment that measured growth rates and reproductive output in wild individuals of a colonial marine invertebrate (Hippopodina iririkiensis), replicated within and across the natural range of succession in its local community. Colony growth rates varied phenotypically throughout this range, but not all such variation was available for selection, nor was it always targeted by selection as expected. While the maintenance of both phenotypic and genetic variation in growth rate is often attributed to costs of growing rapidly, our study highlights the potential for fluctuating selection pressures throughout the life history and across environments to play an important role in this process

Genetic diversity increases population productivity in a sessile marine invertebrate

Reductions in genetic diversity can have widespread ecological consequences: populations with higher genetic diversity are more stable, productive and resistant to disturbance or disease than populations with lower genetic diversity. These ecological effects of genetic diversity differ from the more familiar evolutionary consequences of depleting genetic diversity, because ecological effects manifest within a single generation. If common, genetic diversity effects have the potential to change the way we view and manage populations, but our understanding of these effects is far from complete, and the role of genetic diversity in sexually reproducing animals remains unclear. Here, we examined the effects of genetic diversity in a sexually reproducing marine invertebrate in the field. We manipulated the genetic diversity of experimental populations and then measured individual survival, growth, and fecundity, as well as the size of offspring produced by individuals in high and low genetic diversity populations. Overall, we found greater genetic diversity increased performance across all metrics, and that complementarity effects drove the increased productivity of our highdiversity populations. Our results show that differences in genetic diversity among populations can have pervasive effects on population productivity within remarkably short periods of time

Environmental stress, facilitation, competition, and coexistence

The major theories regarding the combined influence of the environment and species interactions on population and community dynamics appear to conflict. Stress/disturbance gradient models of community organization, such as the stress gradient hypothesis, emphasize a diminished role for competition in harsh environments whereas modern coexistence theory does not. Confusion about the role of species interactions in harsh environments is perpetuated by a disconnect between population dynamics theory and data. We linked theory and data using response surface experiments done in the field to parameterize mathematical, population-dynamic competition models. We replicated our experiment across two environments that spanned a common and important environmental stress gradient for determining community structure in benthic marine systems. We generated quantitative estimates of the effects of environmental stress on population growth rates and the direction and strength of intra- and interspecific interactions within each environment. Our approach directly addressed a perpetual blind spot in this field by showing how the effects of competition can be intensified in stressful environments even though the apparent strength of competition remains unchanged. Furthermore, we showed how simultaneous, reciprocal competitive and facilitative effects can stabilize population dynamics in multispecies communities in stressful environments

Temperature-induced maternal effects and environmental predictability

Maternal effects could influence the persistence of species under environmental change, but the adaptive significance of many empirically estimated maternal effects remains unclear. Inferences about the adaptive significance of maternal effects depend on the correlation between maternal and offspring environments, the relative importance of frequency- or density-dependent selection and whether absolute or relative fitness measures are used. Here, we combine the monitoring of the environment over time with a factorial experiment where we manipulated both the maternal and offspring environment in a marine bryozoan (Bugula neritina). We focused on temperature as our environmental variable as temperature commonly varies over short time scales in nature. We found that offspring from mothers kept in warmer water were smaller and more variable in size, but had increased dispersal potential and higher metamorphic success than offspring from mothers kept in cooler water. Our results suggest that, under frequency- or density-independent selection, mothers that experienced higher temperatures compared with lower temperatures were favoured. Under frequency- or density-dependent selection, there were indications that mothers that experienced higher temperatures would be favoured only if their offspring encountered similar (warmer) temperatures, though these results were not statistically significant. Analysis of time series data on temperature in the field shows that the maternal thermal environment is a good predictor of the temperatures offspring are likely to experience early in life. We suggest that future studies on maternal effects estimate environmental predictability and present both absolute and relative estimates of maternal fitness within each offspring environment

Offspring size variation within broods as a bet-hedging strategy in unpredictable environments

Offspring size is strikingly variable within species. Although theory can account for variation in offspring size among mothers, an adaptive explanation for variation within individual broods has proven elusive. Theoretical considerations of this problem assume that producing offspring that are too small results in reduced offspring viability, but producing offspring that are too large (for that environment) results only in a lost opportunity for increased fecundity. However, logic and recent evidence suggest that offspring above a certain size will also have lower fitness, such that mothers face fitness penalties on either side of an optimum. Although theory assuming intermediate optima has been developed for other diversification traits, the implications of this idea for selection on intra-brood variance in offspring size have not been explored theoretically. Here we model the fitness of mothers producing offspring of uniform vs. variable size in unpredictably variable environments and compare these two strategies under a variety of conditions. Our model predicts that producing variably sized offspring results in higher mean maternal fitness and less variation in fitness among generations when there is a maximum and minimum viable offspring size, and many mothers under- or over-estimate this optimum. This effect is especially strong when the viable offspring size range is narrow relative to the range of environmental variation. To determine whether this prediction is consistent with empirical evidence, we compare within- and among-mother variation in offspring size for 5 phyla of marine invertebrates with different developmental modes corresponding to contrasting levels of environmental predictability. Our comparative analysis reveals that in the developmental mode in which mothers are unlikely to anticipate the relationship between offspring size and performance, size-variation within mothers exceeds variation among mothers, but the converse is true when optimal offspring size is likely to be more predictable. Together, our results support the hypothesis that variation in offspring size within broods can reflect an adaptive strategy for dealing with unpredictably variable environments. We suggest that when there is a minimum and a maximum viable offspring size and the environment is unpredictable, selection will act on both the mean and variance of offspring size

Do Genetic Diversity Effects Drive the Benefits Associated with Multiple Mating? A Test in a Marine Invertebrate

Background: Mothers that mate with multiple males often produce higher quality offspring than mothers that mate with a single male. By engaging in polyandry, mothers may increase their chances of mating with a compatible male or promote sperm competition - both of which act to increase maternal fitness via the biasing of the paternity of offspring. Surprisingly, mating with multiple males, can carry benefits without biasing paternity and may be due simply to differences in genetic diversity between monandrous and polyandrous clutches but role of genetic diversity effects in driving the benefits of polyandry remains poorly tested. Disentangling indirect, genetic benefits from genetic diversity effects is challenging but crucial if we are to understand the selection pressures acting to promote polyandry. Methodology/Principal Findings: Here, we examine the post-fertilisation benefits of accessing the sperm of multiple males in an externally fertilising polychaete worm. Accessing the sperm of multiple males increases offspring performance but this benefit was driven entirely by genetic diversity effects and not by the biasing of paternity at fertilisation. Conclusions/Significance: Previous studies on polyandry should be interpreted cautiously as genetic diversity effects alone can explain the benefits of polyandry yet these diversity effects may be difficult to disentangle from other mechanisms. We suggest that future studies use a modified experimental design in order to discriminate between genetic diversity effects and indirect, genetic benefits

Adaptive paternal effects? Experimental evidence that the paternal environment affects offspring performance

The ability of females to adaptively influence offspring phenotype via maternal effects is widely acknowledged, but corresponding nongenetic paternal effects remain unexplored. Males can adjust sperm phenotype in response to local conditions, but the transgenerational consequences of this plasticity are unknown. We manipulated paternal density of a broadcast spawner (Styela plicata, a solitary ascidean) using methods shown previously to alter sperm phenotype in the field, then conducted in vitro fertilizations that excluded maternal effects and estimated offspring performance under natural conditions. Offspring sired by males from low-density experimental populations developed faster and had a higher hatching success than offspring sired by males living in high densities. In the field, offspring survived relatively better when their environment matched their father's, raising the possibility that fathers can adaptively influence the phenotype of their offspring according to local conditions. As the only difference between offspring is whether they were artificially fertilized by sperm from males kept in high- vs. low-density cages, we can unequivocally attribute any differences in offspring performance to an environmentally induced paternal effect. Males of many species manipulate the phenotype of their sperm in response to sperm competition: our results show this plasticity can influence offspring fitness, potentially in adaptive ways, raising the possibility that adaptive nongenetic paternal effects may be more common than previously thought

Competition in benthic marine invertebrates: the unrecognized role of exploitative competition for oxygen

Competition is a ubiquitous structuring force across systems, but different fields emphasize the role of different types of competition. In benthic marine environments, where some of the classic examples of competition were described, there is a strong emphasis on interference competition: marine invertebrates are assumed to compete fiercely for the limiting resource of space. Much of our understanding of the dynamics of this system is based on this assumption, yet empirical studies often find that increases in density can reduce performance despite free space being available. Furthermore, the assumption that space is the exclusively limiting resource raises paradoxes regarding species coexistence in this system. Here, we measure the availability of oxygen in the field and in the laboratory, as well as the tolerance of resident species to low-oxygen conditions. We show that oxygen can be the primary limiting resource in some instances, and that exploitative competition for this resource is very likely among benthic marine invertebrates. Furthermore, growth form (and the associated risk of oxygen limitation) covaries with the ability to withstand oxygen-poor conditions across a wide range of taxa. Oxygen availability at very small scales may influence the distribution and abundance of sessile marine invertebrates more than is currently appreciated. Furthermore, competition for multiple resources (space and oxygen) and trade-offs in competitive ability for each may promote coexistence in this system

Spatial arrangement affects population dynamics and competition independent of community composition

Theory suggests that the spatial context within which species interactions occur will have major implications for the outcome of competition and ultimately, coexistence, but empirical tests are rare. This is surprising given that individuals of species in real communities are typically distributed nonrandomly in space. Nonrandom spatial arrangement has the potential to modify the relative strength of intra- and interspecific competition by changing the ratio of conspecific to heterospecific competitive encounters, particularly among sessile species where interactions among individuals occur on local scales. Here we test the influence of aggregated and random spatial arrangements on population trajectories of competing species in benthic, marine, sessile-invertebrate assemblages. We show that the spatial arrangement of competing species in simple assemblages has a strong effect on species performance: when conspecifics are aggregated, strong competitors perform poorly and weaker competitors perform better. The effect of specific spatial arrangements depends on species identity but is also strongly context dependent. When there are large differences in species competitive ability, aggregated spatial arrangements can slow competitive exclusion, and so nonrandom spatial arrangement can work synergistically with other trade-off based mechanisms to facilitate coexistence

Offspring size plasticity in response to intraspecific competition: An adaptive maternal effect across life-history stages

When provisioning offspring, mothers balance the benefits of producing a few large, fitter offspring with the costs of decreased fecundity. The optimal balance between offspring size and fecundity depends on the environment. Theory predicts that larger offspring have advantages in adverse conditions, but in favorable conditions size is less important. Thus, if environmental quality varies, selection should favor mothers that adaptively allocate resources in response to local conditions to maximize maternal fitness. In the bryozoan Bugula neritina, we show that the intensity of intraspecific competition dramatically changes the offspring size/performance relationship in the field. In benign or extremely competitive environments, offspring size is less important, but at intermediate levels of competition, colonies from larger larvae have higher performance than colonies from smaller larvae. We predicted mothers should produce larger offspring when intermediate competition is likely and tested these expectations in the field by manipulating the density of brood colonies. Our findings matched expectations: mothers produced larger larvae at high densities and smaller larvae at low densities. In addition, mothers from high‐density environments produced larvae that have higher dispersal potential, which may enable offspring to escape crowded environments. It appears mothers can adaptively adjust offspring size to maximize maternal fitness, altering the offspring phenotype across multiple life‐history stages