A Chromosome-Level Genome Assembly of the Parasitoid Wasp, Cotesia glomerata (Hymenoptera: Braconidae).

Hymenopterans make up about 20% of all animal species, but most are poorly known and lack high-quality genomic resources. One group of important, yet understudied hymenopterans are parasitoid wasps in the family Braconidae. Among this understudied group is the genus Cotesia, a clade of ~1,000 species routinely used in studies of physiology, ecology, biological control, and genetics. However, our ability to understand these organisms has been hindered by a lack of genomic resources. We helped bridge this gap by generating a high-quality genome assembly for the parasitoid wasp, Cotesia glomerata (Braconidae; Microgastrinae). We generated this assembly using multiple sequencing technologies, including Oxford Nanopore, whole-genome shotgun sequencing, and 3D chromatin contact information (HiC). Our assembly is one of the most contiguous, complete, and publicly available hymenopteran genomes, represented by 3,355 scaffolds with a scaffold N50 of ~28 Mb and a BUSCO score of ~99%. Given the genome sizes found in closely related species, our genome assembly was ~50% larger than expected, which was apparently induced by runaway amplification of 3 types of repetitive elements: simple repeats, long terminal repeats, and long interspersed nuclear elements. This assembly is another step forward for genomics across this hyperdiverse, yet understudied order of insects. The assembled genomic data and metadata files are publicly available via Figshare (https://doi.org/10.6084/m9.figshare.13010549).

Balancing selection maintains sex determining alleles in multiple-locus complementary sex determination.

Hymenopteran species in which sex is determined through a haplo-diploid mechanism known as complementary sex determination (CSD) are vulnerable to a unique form of inbreeding depression. Diploids heterozygous at one or more CSD loci develop into females but diploids homozygous at all loci develop into diploid males, which are generally sterile or inviable. Species with multiple polymorphic CSD loci (ml-CSD) may have lower rates of diploid male production than species with a single CSD locus (sl-CSD), but it is not clear if polymorphism is consistently maintained at all loci. Here, we assess the rate of diploid male production in a population of Cotesia rubecula, a two-locus CSD parasitoid wasp species, approximately 20 years after the population was introduced for biological control. We show that diploid male production dropped from 8-13% in 2005 and 2006 to 3-4% by 2015. We also show from experimental crosses that the population maintained polymorphism at both CSD loci in 2015. We use theory and simulations to show that balancing selection on all CSD alleles promotes polymorphism at several loci in ml-CSD populations. Our study supports the hypothesis that ml-CSD populations have lower diploid male production and are more likely to persist than comparable sl-CSD populations.

Effect of Phytoplankton Richness on Phytoplankton Biomass Is Weak Where the Distribution of Herbivores is Patchy.

Positive effects of competitor species richness on competitor productivity can be more pronounced at a scale that includes heterogeneity in 'bottom-up' environmental factors, such as the supply of limiting nutrients. The effect of species richness is not well understood in landscapes where variation in 'top-down' factors, such as the abundance of predators or herbivores, has a strong influence competitor communities. I asked how phytoplankton species richness directly influenced standing phytoplankton biomass in replicate microcosm regions where one patch had a population of herbivores (Daphnia pulicaria) and one patch did not have herbivores. The effect of phytoplankton richness on standing phytoplankton biomass was positive but weak and not statistically significant at this regional scale. Among no-Daphnia patches, there was a significant positive effect of phytoplankton richness that resulted from positive selection effects for two dominant and productive species in polycultures. Among with-Daphnia patches there was not a significant effect of phytoplankton richness. The same two species dominated species-rich polycultures in no- and with-Daphnia patches but both species were relatively vulnerable to consumption by Daphnia. Consistent with previous studies, this experiment shows a measurable positive influence of primary producer richness on biomass when herbivores were absent. It also shows that given the patchy distribution of herbivores at a regional scale, a regional positive effect was not detected.

Intraspecific phenotypic variation in a fish predator affects multitrophic lake metacommunity structure.

Contemporary insights from evolutionary ecology suggest that population divergence in ecologically important traits within predators can generate diversifying ecological selection on local community structure. Many studies acknowledging these effects of intraspecific variation assume that local populations are situated in communities that are unconnected to similar communities within a shared region. Recent work from metacommunity ecology suggests that species dispersal among communities can also influence species diversity and composition but can depend upon the relative importance of the local environment. Here, we study the relative effects of intraspecific phenotypic variation in a fish predator and spatial processes related to plankton species dispersal on multitrophic lake plankton metacommunity structure. Intraspecific diversification in foraging traits and residence time of the planktivorous fish alewife (Alosa pseudoharengus) among coastal lakes yields lake metacommunities supporting three lake types which differ in the phenotype and incidence of alewife: lakes with anadromous, landlocked, or no alewives. In coastal lakes, plankton community composition was attributed to dispersal versus local environmental predictors, including intraspecific variation in alewives. Local and beta diversity of zooplankton and phytoplankton was additionally measured in response to intraspecific variation in alewives. Zooplankton communities were structured by species sorting, with a strong influence of intraspecific variation in A. pseudoharengus. Intraspecific variation altered zooplankton species richness and beta diversity, where lake communities with landlocked alewives exhibited intermediate richness between lakes with anadromous alewives and without alewives, and greater community similarity. Phytoplankton diversity, in contrast, was highest in lakes with landlocked alewives. The results indicate that plankton dispersal in the region supplied a migrant pool that was strongly structured by intraspecific variation in alewives. This is one of the first studies to demonstrate that intraspecific phenotypic variation in a predator can maintain contrasting patterns of multitrophic diversity in metacommunities.

Effects of algal diversity on the production of biomass in homogeneous and heterogeneous nutrient environments: a microcosm experiment.

BACKGROUND: One of the most common questions addressed by ecologists over the past decade has been--how does species richness impact the production of community biomass? Recent summaries of experiments have shown that species richness tends to enhance the production of biomass across a wide range of trophic groups and ecosystems; however, the biomass of diverse polycultures only rarely exceeds that of the single most productive species in a community (a phenomenon called 'transgressive overyielding'). Some have hypothesized that the lack of transgressive overyielding is because experiments have generally been performed in overly-simplified, homogeneous environments where species have little opportunity to express the niche differences that lead to 'complementary' use of resources that can enhance biomass production. We tested this hypothesis in a laboratory experiment where we manipulated the richness of freshwater algae in homogeneous and heterogeneous nutrient environments. METHODOLOGY/PRINCIPAL FINDINGS: Experimental units were comprised of patches containing either homogeneous nutrient ratios (16:1 nitrogen to phosphorus (N:P) in all patches) or heterogeneous nutrient ratios (ranging from 4:1 to 64:1 N:P across patches). After allowing 6-10 generations of algal growth, we found that algal species richness had similar impacts on biomass production in both homo- and heterogeneous environments. Although four of the five algal species showed a strong response to nutrient heterogeneity, a single species dominated algal communities in both types of environments. As a result, a 'selection effect'--where diversity maximizes the chance that a competitively superior species will be included in, and dominate the biomass of a community--was the primary mechanism by which richness influenced biomass in both homo- and heterogeneous environments. CONCLUSIONS/SIGNIFICANCE: Our study suggests that spatial heterogeneity, by itself, is not sufficient to generate strong effects of biodiversity on productivity. Rather, heterogeneity must be coupled with variation in the relative fitness of species across patches in order for spatial niche differentiation to generate complementary resource use.

Impacts of plant diversity on biomass production increase through time because of species complementarity.

Accelerating rates of species extinction have prompted a growing number of researchers to manipulate the richness of various groups of organisms and examine how this aspect of diversity impacts ecological processes that control the functioning of ecosystems. We summarize the results of 44 experiments that have manipulated the richness of plants to examine how plant diversity affects the production of biomass. We show that mixtures of species produce an average of 1.7 times more biomass than species monocultures and are more productive than the average monoculture in 79% of all experiments. However, in only 12% of all experiments do diverse polycultures achieve greater biomass than their single most productive species. Previously, a positive net effect of diversity that is no greater than the most productive species has been interpreted as evidence for selection effects, which occur when diversity maximizes the chance that highly productive species will be included in and ultimately dominate the biomass of polycultures. Contrary to this, we show that although productive species do indeed contribute to diversity effects, these contributions are equaled or exceeded by species complementarity, where biomass is augmented by biological processes that involve multiple species. Importantly, both the net effect of diversity and the probability of polycultures being more productive than their most productive species increases through time, because the magnitude of complementarity increases as experiments are run longer. Our results suggest that experiments to date have, if anything, underestimated the impacts of species extinction on the productivity of ecosystems.

Effects of species diversity on community biomass production change over the course of succession.

Over the past decade an increasing number of studies have experimentally manipulated the number of species in a community and examined how this alters the aggregate production of species biomass. Many of these studies have shown that the effects of richness on biomass change through time, but we have limited understanding of the mechanisms that produce these dynamic trends. Here we report the results of an experiment in which we manipulated the richness of freshwater algae in laboratory microcosms. We used two experimental designs (additive and substitutive) that make different assumptions about how patches are initially colonized, and then tracked the development of community biomass from the point of initial colonization through a period of 6-12 generations of the focal species. We found that the effect of initial species richness on biomass production qualitatively shifted twice over the course of the experiment. The first shift occurred as species transitioned from density-independent to dependent phases of population growth. At this time, intraspecific competition caused monocultures to approach their respective carrying capacities more slowly than polycultures. As a consequence, species tended to over-yield for a brief time, generating a positive, but transient effect of diversity on community biomass. The second shift occurred as communities approached carrying capacity. At this time, strong interspecific interactions caused biomass to be dominated by the competitively superior species in polycultures. As this species had the lowest carrying capacity, a negative effect of diversity on biomass resulted in late succession. Although these two shifts produced dynamics that appeared complex, we show that the patterns can be fit to a simple Lotka-Volterra model of competition. Our results suggest that the effects of algal diversity on primary production change in a predictable sequence through successional time.

Biodiversity as both a cause and consequence of resource availability: a study of reciprocal causality in a predator-prey system.

1. One of the oldest questions in ecology is how species diversity in any given trophic level is related to the availability of essential resources that limit biomass (e.g. water, nutrients, light or prey). Researchers have tried to understand this relationship by focusing either on how diversity is influenced by the availability of resources, or alternatively, how resource abundance is influenced by species diversity. These contrasting perspectives have led to a seeming paradox '... is species diversity the cause or the consequence of resources that limit community biomass?' 2. Here we present results of an experiment that show it is possible for species diversity and resource density to exhibit reciprocal causal relationships in the same ecological system. Using a guild of ladybeetle predators and their aphid prey, we manipulated the number of predator species in field enclosures to examine how predator diversity impacts prey population size. At the same time, we manipulated the abundance of aphid prey in discrete habitat patches within each enclosure to determine how smaller-scale spatial variation in resource abundance affects the number of co-occurring predator species. 3. We found that the number of ladybeetle species added to enclosures had a significant impact on aphid population dynamics because interference competition among the predators reduced per capita rates of predation and, in turn, the overall efficiency of the predator guild. At the same time, spatial variation in aphid abundance among smaller habitat patches generated variation in the observed richness of ladybeetles because more species occurred in patches where predators aggregated in response to high aphid density. 4. The results of our experiment demonstrate that it is possible for species diversity to simultaneously be a cause and a consequence of resource density in the same ecological system, and they shed light on how this might occur for groups of mobile consumers that exhibit rapid responses to spatial and temporal variation in their prey.