Unraveling emergent network indeterminacy in complex ecosystems: A random matrix approach.

Indeterminacy of ecological networks-the unpredictability of ecosystem responses to persistent perturbations-is an emergent property of indirect effects a species has on another through interaction chains. Thus, numerous indirect pathways in large, complex ecological communities could make forecasting the long-term outcomes of environmental changes challenging. However, a comprehensive understanding of ecological structures causing indeterminacy has not yet been reached. Here, using random matrix theory (RMT), we provide mathematical criteria determining whether network indeterminacy emerges across various ecological communities. Our analytical and simulation results show that indeterminacy intricately depends on the characteristics of species interaction. Specifically, contrary to conventional wisdom, network indeterminacy is unlikely to emerge in large competitive and mutualistic communities, while it is a common feature in top-down regulated food webs. Furthermore, we found that predictable and unpredictable perturbations can coexist in the same community and that indeterminate responses to environmental changes arise more frequently in networks where predator-prey relationships predominate than competitive and mutualistic ones. These findings highlight the importance of elucidating direct species relationships and analyzing them with an RMT perspective on two fronts: It aids in 1) determining whether the network's responses to environmental changes are ultimately indeterminate and 2) identifying the types of perturbations causing less predictable outcomes in a complex ecosystem. In addition, our framework should apply to the inverse problem of network identification, i.e., determining whether observed responses to sustained perturbations can reconstruct their proximate causalities, potentially impacting other fields such as microbial and medical sciences.

Are networks of trophic interactions sufficient for understanding the dynamics of multi-trophic communities? Analysis of a tri-trophic insect food-web time-series.

Resource-consumer interactions are considered a major driving force of population and community dynamics. However, species also interact in many non-trophic and indirect ways and it is currently not known to what extent the dynamic coupling of species corresponds to the distribution of trophic links. Here, using a 10-year data set of monthly observations of a 40-species tri-trophic insect community and nonlinear time series analysis, we compare the occurrence and strengths of both the trophic and dynamic interactions in the insect community. The matching between observed trophic and dynamic interactions provides evidence that population dynamic interactions reflect resource-consumer interactions in the many-species community. However, the presence of a trophic interaction does not always correspond to a detectable dynamic interaction especially for top-down effects. Moreover a considerable proportion of dynamic interactions are not attributable to direct trophic interactions, suggesting the unignorable role of non-trophic and indirect interactions as co-drivers of community dynamics.

Density-dependent interspecific interactions and the complexity-stability relationship.

Ever since May theorized that communities with larger numbers of species or interspecific interactions are inherently unstable, the mechanism allowing for the stable existence of complex communities in nature has been a central question in ecology. The main efforts to answer this question have sought to identify non-random features of ecological systems that can reverse a negative complexity-stability relationship into a positive one, but are far from successful, especially in their generality. Here, using the traditional community matrix analysis, we show that variation in the density dependence of interspecific interactions, which should be ubiquitous in nature, can dramatically affect the complexity-stability relationship. More specifically, we reveal that a positive complexity-stability relationship arises when harmful interspecific effects have larger density dependence than beneficial ones, regardless of the signs (i.e. positive or negative) of their dependence. Furthermore, numerical simulations demonstrated the synergistic stabilizing effect of interaction type diversity and density-dependence variation. Thus, this concept of density-dependence variation advances our understanding of the complexity-stability relationship in the real world.

Sexually antagonistic coevolution for sexual harassment can act as a barrier to further invasions by parthenogenesis.

The assumption of a twofold cost of sex not only complicates the maintenance of sex but also sets conditions for sexual conflict: in organisms with the twofold cost, males often sexually harass females. Sexual harassment is detrimental to female fitness and thus might help maintain sexual populations if male harassment inflicts a harsher cost on parthenogens than on sexual females (asymmetric harassment cost). However, the generality of this concept is now considered doubtful because selective harassment of parthenogens results in loss of mating opportunities for males. Using three mathematical models, I show here that sexual harassment still can impose the asymmetric cost on parthenogens. First, I apply the Lotka-Volterra model to show the degree of asymmetric harassment cost that permits sex to be maintained stably in the population. Second, using adaptive dynamics, I examine whether sexually antagonistic coevolution for sexual harassment, which occurs only in sexual populations, can promote the asymmetric harassment cost. Finally, an individual-based model, which assumes a spatial structure unlike that in the other two, demonstrates that the asymmetric evolution of harassment cost prevents further invasions of parthenogens from different patches into sexual lineages; these mechanisms may account for allopatric distributions of sexual and parthenogenetic lineages as well as the maintenance of sex.

Dynamics-based characterization and classification of biodiversity indicators.

Various biodiversity indicators, such as species richness, total abundance, and species diversity indices, have been developed to capture the state of ecological communities over space and time. As biodiversity is a multifaceted concept, it is important to understand the dimension of biodiversity reflected by each indicator for successful conservation and management. Here we utilized the responsiveness of biodiversity indicators' dynamics to environmental changes (i.e., environmental responsiveness) as a signature of the dimension of biodiversity. We present a method for characterizing and classifying biodiversity indicators according to environmental responsiveness and apply the methodology to monitoring data for a marine fish community under intermittent anthropogenic warm water discharge. Our analysis showed that 10 biodiversity indicators can be classified into three super-groups based on the dimension of biodiversity that is reflected. Group I (species richness and community mean of latitudinal center of distribution (cCOD)) showed the greatest robustness to temperature changes; Group II (species diversity and total abundance) showed an abrupt change in the middle of the monitoring period, presumably due to a change in temperature; Group III (species evenness) exhibited the highest sensitivity to environmental changes, including temperature. These results had several ecological implications. First, the responsiveness of species diversity and species evenness to temperature changes might be related to changes in the species abundance distribution. Second, the similar environmental responsiveness of species richness and cCOD implies that fish migration from lower latitudes is a major driver of species compositional changes. The study methodology may be useful in selecting appropriate indicators for efficient biodiversity monitoring.

Reconstruction of a Soil Microbial Network Induced by Stress Temperature.

The microbial community is viewed as a network of diverse microorganisms connected by various interspecific interactions. While the stress gradient hypothesis (SGH) predicts that positive interactions are favored in more stressful environments, the prediction has been less explored in complex microbial communities due to the challenges of identifying interactions. Here, by applying a nonlinear time series analysis to the amplicon-based diversity time series data of the soil microbiota cultured under less stressful (30°C) or more stressful (37°C) temperature conditions, we show how the microbial network responds to temperature stress. While the genera that persisted only under the less stressful condition showed fewer positive effects, the genera that appeared only under the more stressful condition received more positive effects, in agreement with SGH. However, temperature difference also induced reconstruction of the community network, leading to an increased proportion of negative interactions at the whole-community level. The anti-SGH pattern can be explained by the stronger competition caused by increased metabolic rate and population densities. IMPORTANCE By combining amplicon-based diversity survey with recently developed nonlinear analytical tools, we successfully determined the interaction networks of more than 150 natural soil microbial genera under less or more temperature stress and explored the applicability of the stress gradient hypothesis to soil microbiota, shedding new light on the well-known hypothesis.

Field transcriptome revealed a novel relationship between nitrate transport and flowering in Japanese beech.

Recent advances in molecular and genetic studies about flowering time control have been increasingly available to elucidate the physiological mechanism underlying masting, the intermittent and synchronized production of a large amount of flowers and seeds in plant populations. To identify unexplored developmental and physiological processes associated with masting, genome-wide transcriptome analysis is a promising tool, but such analyses have yet to be performed. We established a field transcriptome using a typical masting species, Japanese beech (Fagus crenata Blume), over two years, and analyzed the data using a nonlinear time-series analysis called convergent cross mapping. Our field transcriptome was found to undergo numerous changes depending on the status of floral induction and season. An integrated approach of high-throughput transcriptomics and causal inference was successful at detecting novel causal regulatory relationships between nitrate transport and florigen synthesis/transport in a forest tree species. The synergistic activation of nitrate transport and floral transition could be adaptive to simultaneously satisfy floral transition at the appropriate timing and the nitrogen demand needed for flower formation.

Ecological effects of sex differ with trophic positions in a simple food web.

Sexual differences in parental investment, predation pressure, and foraging efforts are common in nature and affect the trophic flow in food webs. Specifically, the sexual differences in predator and prey behavior change in trophic inflow and outflow, respectively, while those in parental investment alter the reproductive allocation of acquired resources in the population. Consequently, these factors may play an important role in determining the system structure and persistence. However, few studies have examined how sexual differences in trophic flow affect food web dynamics. In this study, I show the ecological role of sex by explicitly incorporating sexual differences in trophic flow into a three-species food web model. The results demonstrated that the ecological waste of males, that is, the amount of trophic inflow into males with less parental investment, plays an important role in system persistence and structure. In particular, the synergy between sexual differences in parental investment and trophic inflows and outflows is important in determining web persistence: Significant impacts of male-biased trophic flows require the condition of anisogamy. In addition, the dynamic effects of the ecological waste of males differ with trophic level: The coexistence of a food web occurs more frequently with biased inflows into predator males, but occurs less frequently with biased inflows into consumer males. The model analysis indicates that investigating the pattern of sexual differences among trophic positions can enrich our understanding of food web persistence and structure in the real world.

Red Queen dancing in the lek: effects of mating skew on host-parasite interactions.

The RQH (Red Queen hypothesis), which argues that hosts need to be continuously finding new ways to avoid parasites that are able to infect common host genotypes, has been at the center of discussions on the maintenance of sex. This is because diversity is favored under the host-parasite coevolution based on negative frequency-dependent selection, and sexual reproduction is a mechanism that generates genetic diversity in the host population. Together with parasite infections, sexual organisms are usually under sexual selection, which leads to mating skew or mating success biased toward males with a particular phenotype. Thus, strong mating skew would affect genetic variance in a population and should affect the benefit of the RQH. However, most models have investigated the RQH under a random mating system and not under mating skew. In this study, I show that sexual selection and the resultant mating skew may increase parasite load in the hosts. An IBM (individual-based model), which included host-parasite interactions and sexual selection among hosts, demonstrates that mating skew influenced parasite infection in the hosts under various conditions. Moreover, the IBM showed that the mating skew evolves easily in cases of male-male competition and female mate choice, even though it imposes an increased risk of parasite infection on the hosts. These findings indicated that whether the RQH favored sexual reproduction depended on the condition of mating skew. That is, consideration of the host mating system would provide further understanding of conditions in which the RQH favors sexual reproduction in real organisms.

Sexual conflict over the maintenance of sex: effects of sexually antagonistic coevolution for reproductive isolation of parthenogenesis.

Sexual reproduction involves many costs. Therefore, females acquiring a capacity for parthenogenetic (or asexual) reproduction will gain a reproductive advantage over obligately sexual females. In contrast, for males, any trait coercing parthenogens into sexual reproduction (male coercion) increases their fitness and should be under positive selection because parthenogenesis deprives them of their genetic contribution to future generations. Surprisingly, although such sexual conflict is a possible outcome whenever reproductive isolation is incomplete between parthenogens and the sexual ancestors, it has not been given much attention in the studies of the maintenance of sex. Using two mathematical models, I show here that the evolution of male coercion substantially favours the maintenance of sex even though a female barrier against the coercion can evolve. First, the model based on adaptive-dynamics theory demonstrates that the resultant antagonistic coevolution between male coercion and a female barrier fundamentally ends in either the prevalence of sex or the co-occurrence of two reproductive modes. This is because the coevolution between the two traits additionally involves sex-ratio selection, that is, an increase in parthenogenetic reproduction leads to a female-biased population sex ratio, which will enhance reproductive success of more coercive males and directly promotes the evolution of the coercion among males. Therefore, as shown by the individual-based model, the establishment of obligate parthenogenesis in the population requires the simultaneous evolution of strong reproductive isolation between males and parthenogens. These findings should shed light on the interspecific diversity of reproductive modes as well as help to explain the prevalence of sexual reproduction.

Sex ratio biases in termites provide evidence for kin selection.

Inclusive fitness theory, also known as kin selection theory, is the most general expansion of Darwin's natural selection theory. It is supported by female-biased investment by workers in the social Hymenoptera where relatedness to sisters is higher than to brothers because of haplodiploidy. However, a strong test of the theory has proven difficult in diploid social insects because they lack such relatedness asymmetry. Here we show that kin selection can result in sex ratio bias in eusocial diploids. Our model predicts that allocation will be biased towards the sex that contributes more of its genes to the next generation when sex-asymmetric inbreeding occurs. The prediction matches well with the empirical sex allocation of Reticulitermes termites where the colony king can be replaced by a queen's son. Our findings open broad new avenues to test inclusive fitness theory beyond the well-studied eusocial Hymenoptera.

Queen succession through asexual reproduction in termites.

The evolution and maintenance of sexual reproduction may involve important tradeoffs because asexual reproduction can double an individual's contribution to the gene pool but reduces diversity. Moreover, in social insects the maintenance of genetic diversity among workers may be important for colony growth and survival. We identified a previously unknown termite breeding system in which both parthenogenesis and sexual reproduction are conditionally used. Queens produce their replacements asexually but use normal sexual reproduction to produce other colony members. These findings show how eusociality can lead to extraordinary reproductive systems and provide important insights into the advantages and disadvantages of sex.