The role of phenotypic plasticity in shaping ecological networks.

Plasticity-mediated changes in interaction dynamics and structure may scale up and affect the ecological network in which the plastic species are embedded. Despite their potential relevance for understanding the effects of plasticity on ecological communities, these effects have seldom been analysed. We argue here that, by boosting the magnitude of intra-individual phenotypic variation, plasticity may have three possible direct effects on the interactions that the plastic species maintains with other species in the community: may expand the interaction niche, may cause a shift from one interaction niche to another or may even cause the colonization of a new niche. The combined action of these three factors can scale to the community level and eventually expresses itself as a modification in the topology and functionality of the entire ecological network. We propose that this causal pathway can be more widespread than previously thought and may explain how interaction niches evolve quickly in response to rapid changes in environmental conditions. The implication of this idea is not solely eco-evolutionary but may also help to understand how ecological interactions rewire and evolve in response to global change.

Phenotypic plasticity guides Moricandia arvensis divergence and convergence across the Brassicaceae floral morphospace.

Many flowers exhibit phenotypic plasticity. By inducing the production of several phenotypes, plasticity may favour the rapid exploration of different regions of the floral morphospace. We investigated how plasticity drives Moricandia arvensis, a species displaying within-individual floral polyphenism, across the floral morphospace of the entire Brassicaceae family. We compiled the multidimensional floral phenotype, the phylogenetic relationships, and the pollination niche of over 3000 species to construct a family-wide floral morphospace. We assessed the disparity between the two M. arvensis floral morphs (as the distance between the phenotypic spaces occupied by each morph) and compared it with the family-wide disparity. We measured floral divergence by comparing disparity with the most common ancestor, and estimated the convergence of each floral morph with other species belonging to the same pollination niches. Moricandia arvensis exhibits a plasticity-mediated floral disparity greater than that found between species, genera and tribes. The novel phenotype of M. arvensis moves outside the region occupied by its ancestors and relatives, crosses into a new region where it encounters a different pollination niche, and converges with distant Brassicaceae lineages. Our study suggests that phenotypic plasticity favours floral divergence and rapid appearance of convergent flowers, a process which facilitates the evolution of generalist pollination systems.

The phylogenetic roots of human lethal violence.

The psychological, sociological and evolutionary roots of conspecific violence in humans are still debated, despite attracting the attention of intellectuals for over two millennia. Here we propose a conceptual approach towards understanding these roots based on the assumption that aggression in mammals, including humans, has a significant phylogenetic component. By compiling sources of mortality from a comprehensive sample of mammals, we assessed the percentage of deaths due to conspecifics and, using phylogenetic comparative tools, predicted this value for humans. The proportion of human deaths phylogenetically predicted to be caused by interpersonal violence stood at 2%. This value was similar to the one phylogenetically inferred for the evolutionary ancestor of primates and apes, indicating that a certain level of lethal violence arises owing to our position within the phylogeny of mammals. It was also similar to the percentage seen in prehistoric bands and tribes, indicating that we were as lethally violent then as common mammalian evolutionary history would predict. However, the level of lethal violence has changed through human history and can be associated with changes in the socio-political organization of human populations. Our study provides a detailed phylogenetic and historical context against which to compare levels of lethal violence observed throughout our history.

Killing conspecific adults in mammals.

Mammals kill both conspecific infants and adults. Whereas infanticide has been profusely studied, the killing of non-infants (adulticide) has seldom attracted the attention of researchers. Mammals kill conspecific adults by at least four, non-exclusive reasons: during intrasexual aggression for mating opportunities, to defend valuable resources, to protect their progeny and to prey upon conspecifics. In this study, we test which reason is most likely to explain male and female adulticide in mammals. For this, we recorded the presence of adulticide, the ecological and behavioural traits, and the phylogenetic relationship for more than 1000 species. Adulticide has been recorded in over 350 species from the most important Mammalian clades. Male adulticide was phylogenetically correlated with the presence of size dimorphism and intrasexually selected weapons. Female adulticide was phylogenetically associated with the occurrence of infanticide. These results indicate that the evolutionary pathways underlying the evolution of adulticide differ between sexes in mammals. Whereas males commit adulticide to increase breeding opportunities and to compete with other males for mating, females commit adulticide mainly to defend offspring from infanticidal conspecifics.

Pre-dispersal seed predators boost seed production in a short-lived plant.

Pre-dispersal seed predation diminishes fitness and population growth rate of many plant species. Therefore, plants have developed multiple strategies to reduce the harmful effects of this type of herbivory. The present study aims to determine the effect of pre-dispersal seed predators (PSPs) on the fitness of a short-lived herb, and to discern the mechanisms allowing the plants to reduce the impact of pre-dispersal seed predation. Knowing that the interplay between pre-dispersal seed predators and plants is strongly shaped by the presence of other co-occurring organisms, we tested whether detritivores modulate plant responses towards pre-dispersal seed predators. To do so, we experimentally manipulated in the field pre-dispersal seed predators and detritivores interacting with the short-lived herb Moricandia moricandioides. We found that detritivores did not alter the response of plants to PSPs. Strikingly, the plant overcompensated for pre-dispersal seed predation, almost doubling the number of seeds produced. Plant response to PSPs led to substantial changes in shoot architecture, reproductive traits, chemical defences in leaves and seeds and in seed nutrient content. The overcompensating mechanism seems to be meristem activation, which allowed plants to produce more reproductive tissue, and increasing the proportion of ovules that became seeds, a response which specifically compensates for pre-dispersal seed predation. As far as we know, this is the first experimental evidence of a positive effect of PSPs on plant lifetime fitness as a consequence of plant overcompensation.

Within- and trans-generational effects of herbivores and detritivores on plant performance and reproduction.

Mutualistic and antagonistic above-ground and below-ground species have the potential to be involved in strong interactions that can either weaken or strengthen their individual impacts on plants. Their impacts can also have delayed effects on a plant's progeny by altering offspring traits and survival. Few studies have explored the effect of herbivore and detritivore interactions with parent plants on offspring vital life-cycle processes, such as seedling emergence rate, seedling establishment and offspring survival. In the field, I experimentally studied the combined effects of floral herbivores (FH), root herbivores (RH) and detritivores on plant growth and reproduction of Moricandia moricandioides (Brassicaceae). In particular, I analysed the trans-generational effects of herbivores and detritivores on seed and juvenile production as well as on vital life-cycle processes (i.e. seedling emergence rates, survival). Floral herbivores strongly reduced the number of flowers, fruits, seeds and juveniles. Detritivores had an impact on plant success by increasing seed quality (% N and N : C ratio), although the effect was altered by the presence of floral and RH. I found maternal effects (trans-generational effects) of FH, RH and detritivores. Floral herbivores reduced seedling emergence and establishment. Floral and RH in combination reduced seedling emergence timing, but the effect was counteracted by detritivores. Detritivores also reduced the negative effect of FH on offspring mortality rate. This study shows that the impact of above-ground and below-ground organisms on M. moricandioides plants go beyond seed production and were evident in the probability of establishment and survival of the following generation. Trans-generational effects were induced by all three groups of interacting organisms and the net consequences for plant offspring depended on the organisms interacting with the plant.

Density-Dependent Effects of Simultaneous Root and Floral Herbivory on Plant Fitness and Defense.

Plants are attacked by multiple herbivores, and depend on a precise regulation of responses to cope with a wide range of antagonists. Simultaneous herbivory can occur in different plant compartments, which may pose a serious threat to plant growth and reproduction. In particular, plants often face co-occurring root and floral herbivory, but few studies have focused on such interactions. Here, we investigated in the field the combined density-dependent effects of root-chewing cebrionid beetle larvae and flower-chewing pierid caterpillars on the fitness and defense of a semiarid Brassicaceae herb. We found that the fitness impact of both herbivore groups was independent and density-dependent. Increasing root herbivore density non-significantly reduced plant fitness, while the relationship between increasing floral herbivore density and the reduction they caused in both seed number and seedling emergence was non-linear. The plant defensive response was non-additive with regard to the different densities of root and floral herbivores; high floral herbivore density provoked compensatory investment in reproduction, and this tolerance response was combined with aboveground chemical defense induction when also root herbivore density was high. Plants may thus prioritize specific trait combinations in response to varying combined below- and aboveground herbivore densities to minimize negative impacts on fitness.

Within-individual phenotypic plasticity in flowers fosters pollination niche shift.

Phenotypic plasticity, the ability of a genotype of producing different phenotypes when exposed to different environments, may impact ecological interactions. We study here how within-individual plasticity in Moricandia arvensis flowers modifies its pollination niche. During spring, this plant produces large, cross-shaped, UV-reflecting lilac flowers attracting mostly long-tongued large bees. However, unlike most co-occurring species, M. arvensis keeps flowering during the hot, dry summer due to its plasticity in key vegetative traits. Changes in temperature and photoperiod in summer trigger changes in gene expression and the production of small, rounded, UV-absorbing white flowers that attract a different assemblage of generalist pollinators. This shift in pollination niche potentially allows successful reproduction in harsh conditions, facilitating M. arvensis to face anthropogenic perturbations and climate change.

Characterization of microsatellite markers for Moricandia moricandioides (Brassicaceae) and related species.

PREMISE OF THE STUDY: Polymorphic microsatellite markers were developed to study population structure and mating patterns of the monocarpic herb Moricandia moricandioides (Brassicaceae). METHODS AND RESULTS: Illumina MiSeq sequencing was used to develop a panel of 15 polymorphic microsatellite markers that were tested across 77 individuals from three populations on the Iberian Peninsula. All markers were polymorphic in at least two studied populations, and the number of alleles ranged from one to 11 per locus. The levels of observed and expected heterozygosity ranged from 0.000 to 1.000 and from 0.153 to 0.865, respectively. Nine and 11 loci were successfully amplified in the congeneric species M. arvensis and M. foetida, respectively. CONCLUSIONS: The 15 microsatellite markers will be useful for population genetic studies of the genus Moricandia. These markers will serve as a useful tool for exploring population structure and mating patterns of M. moricandioides.

Transgenerational effects of ungulates and pre-dispersal seed predators on offspring success and resistance to herbivory.

Herbivorous mammals and insect pre-dispersal seed predators are two types of herbivores that, despite their functional and morphological differences, tend to severely impact many plant species, highly decreasing their seed production and even imperiling the performance of their offspring through transgenerational effects. However, how they influence offspring resistance to herbivory remains largely unknown. In this study we experimentally examined the effects of ungulates and pre-dispersal seed predators on seed quality as well as on the emergence, survival and resistance to herbivory of the seedlings of a semiarid herb. We found that ungulates reduced seedling recruitment but increased seedling resistance to leaf miners. These effects were probably a consequence of insufficient carbon provisioning in seeds that reduced seed viability and provoked carbon limitation in seedlings. Pre-dispersal seed predators did not influence seedling recruitment, but seedlings from mothers damaged by ungulates and by pre-dispersal seed predators suffered less herbivory by grasshoppers. Remarkably, intra-individual differences in damage by pre-dispersal seed predators affected the rate of damage underwent by seedlings. That is, seedlings derived from fruits attacked by seed predators were more resistant to herbivores than siblings derived from un-attacked fruits in plant populations exposed to ungulates. To our knowledge, this is the first study reporting variation in transgenerational-induced resistance of seedlings from the same maternal plant. This study is a valuable contribution to the understanding of transgenerational effects of multiple herbivores and their implications for a deeper comprehension of the natural systems in which they co-occur.

Direct and indirect effects of climate and habitat factors on butterfly diversity.

Many factors, including climate, resource availability, and habitat diversity, have been proposed as determinants of global diversity, but the links among them have rarely been studied. Using structural equation modeling (SEM), we investigated direct and indirect effects of climate variables, host-plant richness, and habitat diversity on butterfly species richness across Britain, at 20-km grid resolution. These factors were all important determinants of butterfly diversity, but their relative contributions differed between habitat generalists and specialists, and whether the effects were direct or indirect. Climate variables had strong effects on habitat generalists, whereas host-plant richness and habitat diversity contributed relatively more for habitat specialists. Considering total effects (direct and indirect together), climate variables had the strongest link to butterfly species richness for all groups of species. The results suggest that different mechanistic hypotheses to explain species richness may be more appropriate for habitat generalists and specialists, with generalists hypothesized to show direct physiological limitations and specialists additionally being constrained by trophic interactions (climate affecting host-plant richness).

Molecular phylogeny and evolutionary history of Moricandia DC (Brassicaceae).

BACKGROUND: The phylogeny of tribe Brassiceae (Brassicaceae) has not yet been resolved because of its complex evolutionary history. This tribe comprises economically relevant species, including the genus Moricandia DC. This genus is currently distributed in North Africa, Middle East, Central Asia and Southern Europe, where it is associated with arid and semi-arid environments. Although some species of Moricandia have been used in several phylogenetic studies, the phylogeny of this genus is not well established. METHODS: Here we present a phylogenetic analysis of the genus Moricandia using a nuclear (the internal transcribed spacers of the ribosomal DNA) and two plastidial regions (parts of the NADH dehydrogenase subunit F gene and the trnT-trnF region). We also included in the analyses members of their sister genus Rytidocarpus and from the close genus Eruca. RESULTS: The phylogenetic analyses showed a clear and robust phylogeny of the genus Moricandia. The Bayesian inference tree was concordant with the maximum likelihood and timing trees, with the plastidial and nuclear trees showing only minor discrepancies. The genus Moricandia appears to be formed by two main lineages: the Iberian clade including three species, and the African clade including the four species inhabiting the Southern Mediterranean regions plus M. arvensis. DISCUSSION: We dated the main evolutionary events of this genus, showing that the origin of the Iberian clade probably occurred after a range expansion during the Messinian period, between 7.25 and 5.33 Ma. In that period, an extensive African-Iberian floral and faunal interchange occurred due to the existence of land bridges between Africa and Europa in what is, at present-days, the Strait of Gibraltar. We have demonstrated that a Spanish population previously ascribed to Rytidocarpus moricandioides is indeed a Moricandia species, and we propose to name it as M. rytidocarpoides sp. nov. In addition, in all the phylogenetic analyses, M. foleyi appeared outside the Moricandia lineage but within the genus Eruca. Therefore, M. foleyi should be excluded from the genus Moricandia and be ascribed, at least provisionally, to the genus Eruca.

Climate change effects on above- and below-ground interactions in a dryland ecosystem.

Individual species respond to climate change by altering their abundance, distribution and phenology. Less is known, however, about how climate change affects multitrophic interactions, and its consequences for food-web dynamics. Here, we investigate the effect of future changes in rainfall patterns on detritivore-plant-herbivore interactions in a semiarid region in southern Spain by experimentally manipulating rainfall intensity and frequency during late spring-early summer. Our results show that rain intensity changes the effect of below-ground detritivores on both plant traits and above-ground herbivore abundance. Enhanced rain altered the interaction between detritivores and plants affecting flower and fruit production, and also had a direct effect on fruit and seed set. Despite this finding, there was no net effect on plant reproductive output. This finding supports the idea that plants will be less affected by climatic changes than by other trophic levels. Enhanced rain also affected the interaction between detritivores and free-living herbivores. The effect, however, was apparent only for generalist and not for specialist herbivores, demonstrating a differential response to climate change within the same trophic level. The complex responses found in this study suggest that future climate change will affect trophic levels and their interactions differentially, making extrapolation from individual species' responses and from one ecosystem to another very difficult.

Effects of brood parasitism on host reproductive success: evidence from larval interactions among dung beetles.

This paper investigates the effect of brood parasitism in a dung beetle assemblage in an arid region of Spain. The study was conducted during the spring season (March-May 1994-1998) using mesh cylinders buried into the ground, filled with sand and with sheep dung on top. We quantified the proportion of nests containing larvae of parasitic beetles and their effect on host larvae survival. Experiments on the effect of parasitic larvae on host-larvae survival were conducted by placing scarab brood masses (raised from captive scarabs in the laboratory) in containers with and without aphodiid larvae. During the spring, dung desiccation is rapid, preventing aphodiids nesting in the dung, and forcing these species to adopt brood parasitism as a nesting strategy. Parasitic aphodiids were found in 12-47% of scarab nests of three species. The incidence of brood parasitization was positively related with the number of brood masses contained in the nests, being also higher in the most abundant species. Field data and experiments showed that brood parasites significantly reduced host larvae survival from 74.8% in non-parasitized nests to 8.8% in parasitized nests. Because different rates of nest parasitization and mortality were caused by parasites, brood parasitism had a differential effect on different host species. Thus, brood parasitism constitutes an important mortality factor reducing the reproductive success of the host species and potentially affecting the beetle abundance in the area.