Using text-mined trait data to test for cooperate-and-radiate co-evolution between ants and plants.

Mutualisms may be "key innovations" that spur lineage diversification by augmenting niche breadth, geographic range, or population size, thereby increasing speciation rates or decreasing extinction rates. Whether mutualism accelerates diversification in both interacting lineages is an open question. Research suggests that plants that attract ant mutualists have higher diversification rates than non-ant associated lineages. We ask whether the reciprocal is true: does the interaction between ants and plants also accelerate diversification in ants, i.e. do ants and plants cooperate-and-radiate? We used a novel text-mining approach to determine which ant species associate with plants in defensive or seed dispersal mutualisms. We investigated patterns of lineage diversification across a recent ant phylogeny using BiSSE, BAMM, and HiSSE models. Ants that associate mutualistically with plants had elevated diversification rates compared to non-mutualistic ants in the BiSSE model, with a similar trend in BAMM, suggesting ants and plants cooperate-and-radiate. However, the best-fitting model was a HiSSE model with a hidden state, meaning that diversification models that do not account for unmeasured traits are inappropriate to assess the relationship between mutualism and ant diversification. Against a backdrop of diversification rate heterogeneity, the best-fitting HiSSE model found that mutualism actually decreases diversification: mutualism evolved much more frequently in rapidly diversifying ant lineages, but then subsequently slowed diversification. Thus, it appears that ant lineages first radiated, then cooperated with plants.

Dominance-diversity relationships in ant communities differ with invasion.

The relationship between levels of dominance and species richness is highly contentious, especially in ant communities. The dominance-impoverishment rule states that high levels of dominance only occur in species-poor communities, but there appear to be many cases of high levels of dominance in highly diverse communities. The extent to which dominant species limit local richness through competitive exclusion remains unclear, but such exclusion appears more apparent for non-native rather than native dominant species. Here we perform the first global analysis of the relationship between behavioral dominance and species richness. We used data from 1,293 local assemblages of ground-dwelling ants distributed across five continents to document the generality of the dominance-impoverishment rule, and to identify the biotic and abiotic conditions under which it does and does not apply. We found that the behavioral dominance-diversity relationship varies greatly, and depends on whether dominant species are native or non-native, whether dominance is considered as occurrence or relative abundance, and on variation in mean annual temperature. There were declines in diversity with increasing dominance in invaded communities, but diversity increased with increasing dominance in native communities. These patterns occur along the global temperature gradient. However, positive and negative relationships are strongest in the hottest sites. We also found that climate regulates the degree of behavioral dominance, but differently from how it shapes species richness. Our findings imply that, despite strong competitive interactions among ants, competitive exclusion is not a major driver of local richness in native ant communities. Although the dominance-impoverishment rule applies to invaded communities, we propose an alternative dominance-diversification rule for native communities.

A global database of ant species abundances.

What forces structure ecological assemblages? A key limitation to general insights about assemblage structure is the availability of data that are collected at a small spatial grain (local assemblages) and a large spatial extent (global coverage). Here, we present published and unpublished data from 51 ,388 ant abundance and occurrence records of more than 2,693 species and 7,953 morphospecies from local assemblages collected at 4,212 locations around the world. Ants were selected because they are diverse and abundant globally, comprise a large fraction of animal biomass in most terrestrial communities, and are key contributors to a range of ecosystem functions. Data were collected between 1949 and 2014, and include, for each geo-referenced sampling site, both the identity of the ants collected and details of sampling design, habitat type, and degree of disturbance. The aim of compiling this data set was to provide comprehensive species abundance data in order to test relationships between assemblage structure and environmental and biogeographic factors. Data were collected using a variety of standardized methods, such as pitfall and Winkler traps, and will be valuable for studies investigating large-scale forces structuring local assemblages. Understanding such relationships is particularly critical under current rates of global change. We encourage authors holding additional data on systematically collected ant assemblages, especially those in dry and cold, and remote areas, to contact us and contribute their data to this growing data set.

Climate mediates the effects of disturbance on ant assemblage structure.

Many studies have focused on the impacts of climate change on biological assemblages, yet little is known about how climate interacts with other major anthropogenic influences on biodiversity, such as habitat disturbance. Using a unique global database of 1128 local ant assemblages, we examined whether climate mediates the effects of habitat disturbance on assemblage structure at a global scale. Species richness and evenness were associated positively with temperature, and negatively with disturbance. However, the interaction among temperature, precipitation and disturbance shaped species richness and evenness. The effect was manifested through a failure of species richness to increase substantially with temperature in transformed habitats at low precipitation. At low precipitation levels, evenness increased with temperature in undisturbed sites, peaked at medium temperatures in disturbed sites and remained low in transformed sites. In warmer climates with lower rainfall, the effects of increasing disturbance on species richness and evenness were akin to decreases in temperature of up to 9°C. Anthropogenic disturbance and ongoing climate change may interact in complicated ways to shape the structure of assemblages, with hot, arid environments likely to be at greatest risk.

How many and which ant species are being accidentally moved around the world?

Human transportation facilitates the dispersal of exotic ants, but few studies have quantified the magnitude and geography of these movements. We used several non-parametric indices to estimate the number of species successfully introduced to or established in new regions. We also compared their source biogeographic realms to assess the importance of geographical origin in determining the likelihood of establishment after introduction. Occurrence data on exotic ants derive from studies of three temperate regions. Our results suggest that the numbers of introduced or established ants may be much larger than the numbers so far documented. Ants introduced or established in new regions tend to arrive from the same or neighbouring realms, as would be expected if exotic species tend to match climates and if arrival/establishment is dependent upon higher trade rates from neighbouring countries.

Relative roles of climatic suitability and anthropogenic influence in determining the pattern of spread in a global invader.

Because invasive species threaten the integrity of natural ecosystems, a major goal in ecology is to develop predictive models to determine which species may become widespread and where they may invade. Indeed, considerable progress has been made in understanding the factors that influence the local pattern of spread for specific invaders and the factors that are correlated with the number of introduced species that have become established in a given region. However, few studies have examined the relative importance of multiple drivers of invasion success for widespread species at global scales. Here, we use a dataset of >5,000 presence/absence records to examine the interplay between climatic suitability, biotic resistance by native taxa, human-aided dispersal, and human modification of habitats, in shaping the distribution of one of the world's most notorious invasive species, the Argentine ant (Linepithema humile). Climatic suitability and the extent of human modification of habitats are primarily responsible for the distribution of this global invader. However, we also found some evidence for biotic resistance by native communities. Somewhat surprisingly, and despite the often cited importance of propagule pressure as a crucial driver of invasions, metrics of the magnitude of international traded commodities among countries were not related to global distribution patterns. Together, our analyses on the global-scale distribution of this invasive species provide strong evidence for the interplay of biotic and abiotic determinants of spread and also highlight the challenges of limiting the spread and subsequent impact of highly invasive species.

How many and which ant species are being accidentally moved around the world?

Human transportation facilitates the dispersal of exotic ants, but few studies have quantified the magnitude and geography of these movements. We used several non-parametric indexes to estimate the number of species successfully introduced to or established in new regions. We also compared their source biogeographic realms to assess the importance of the geographical origin in determining the likelihood of establishment after introduction. Data on exotic ants derive from studies of three temperate regions. Our results suggest that the numbers of introduced or established ants may be much larger than the numbers so far documented. Ants introduced or established in new regions tend to arrive from the same or neighbouring realms, as would be expected if exotic species tend to match climates and if arrival/establishment is dependent upon higher trade rates from neighbouring countries.

Effect of temperature on the development and survival of the Argentine ant, Linepithema humile.

The influence of temperature on the developmental times and survival of insects can largely determine their distribution. For invasive species, like the Argentine ant, Linepithema humile Mayr (Hymenoptera: Formicidae), these data are essential for predicting their potential range based on mechanistic models. In the case of this species, such data are too scarce and incomplete to make accurate predictions based on its physiological needs. This research provides comprehensive new data about brood survival and developmental times at a wide range of temperatures under laboratory conditions. Temperature affected both the complete brood development from egg to adult worker and each of the immature stages separately. The higher the temperature, the shorter the development times. Brood survival from egg to adult was low, with the maximum survival rate being only 16% at 26 degrees C. Temperature also affected survival of each of the immature stages differently: eggs were negatively affected by high temperatures, while larvae were negatively affected by low temperatures, and the survival of pupae was apparently independent of environmental temperature. At 32 degrees C no eggs survived, while at 18 degrees C less than 2% of the eggs hatched into larva. The data from the present study are essential for developing prediction models about the distribution range of this tramp species based on its physiological needs in relation to temperature.

Reproductive inhibition among nestmate queens in the invasive Argentine ant.

In social species, the presence of several reproductive individuals can generate conflict. In social insects, as queen number increases, individual oviposition rate may decrease because of direct and indirect behavioural and/or chemical interactions. Understanding the factors that mediate differences in queen fecundity should provide insight into the regulation and maintenance of highly polygynous insect societies, such as those of the invasive Argentine ant (Linepithema humile). In this study, we investigated (1) whether differences in the oviposition rates of Argentine ant queens exposed to polygynous conditions could result from interactions among them; (2) whether such differences in fecundity stemmed from differences in worker attention; and (3) whether polygynous conditions affected the cuticular hydrocarbon profiles of queens (CHCs). We found that differences in queen fecundity and CHC profiles observed under polygynous conditions disappeared when queens were exposed to monogynous conditions, suggesting some form of reproductive inhibition may exist when queens cohabit. These differences did not seem to arise from variation in worker attention because more fecund queens were not more attractive to workers. Levels of some CHCs were higher in more fecund queens. These CHCs are associated with greater queen productivity and survival. Our findings indicate that such compounds could be multifunctional queen pheromones.

Factors triggering queen executions in the Argentine ant.

Competition among queens in polygynous societies may result in queen executions or conflicts over personal reproduction. Understanding the factors that mediate the executions of ant queens should provide insight into how queen numbers are regulated in polygynous insect societies. The Argentine ant is a widespread invasive species that displays secondary polygyny, and workers execute 90% of their nestmate queens each spring. In this study, we investigated: (1) whether ambient temperature, queen number, and protein deprivation have an effect on queen executions and (2) whether workers select the queens slated for execution based on their cuticular hydrocarbon (CHC) profiles. We found that the percentage of queens executed was positively correlated with temperature and queen number but that protein deprivation did not play a role. As for queen fate, the levels of some CHCs were higher in surviving queens. One of these CHCs is associated with queen productivity (i.e egg-laying rate and ovarian index) suggesting that workers execute the least productive queens. Our findings suggest that chemical cues related to fertility signaling may mediate queen executions in Argentine ants.

Effect of temperature on the oviposition rate of Argentine ant queens (Linepithema humile Mayr) under monogynous and polygynous experimental conditions.

Data concerning the influence of temperature on a species' physiological parameters can be a useful tool for predicting its potential distribution range, but in the case of the Argentine ant, data based on its physiological needs are too scarce and incomplete to make accurate predictions of this type. In the present study, we offer new and complete data concerning the Argentine ant queen's oviposition rate under a wide range of temperatures in the laboratory. We analyzed the oviposition rate of the Argentine ant (Linepithema humile) at 12 experimental temperatures: 10, 12, 14, 16, 18, 21, 24, 26, 28, 30, 32 and 34 degrees C under monogynous conditions (one queen per nest) and three different polygynous conditions (two, four and eight queens per nest). We found that temperature affected their oviposition rate and that the effect was similar regardless of the number of queens in the nest. Egg laying was at its maximum at 28 degrees C, with variation in the upper and lower temperature limits at which oviposition took place depending on the degree of polygyny. Oviposition rates were negatively correlated with the number of queens in the nest. We also observed a marked variation in the oviposition rate of queens subjected to the same experimental conditions.

Cuticular hydrocarbons correlate with queen reproductive status in native and invasive Argentine ants (Linepithema humile, Mayr).

In insect societies, chemical communication plays an important role in colony reproduction and individual social status. Many studies have indicated that cuticular hydrocarbons (CHCs) are the main chemical compounds encoding reproductive status. However, these studies have largely focused on queenless or monogynous species whose workers are capable of egg laying and have mainly explored the mechanisms underlying queen-worker or worker-worker reproductive conflicts. Less is known about what occurs in highly polygynous ant species with permanently sterile workers. Here, we used the Argentine ant as a model to examine the role of CHCs in communicating reproductive information in such insect societies. The Argentine ant is unicolonial, highly polygynous, and polydomous. We identified several CHCs whose presence and levels were correlated with queen age, reproductive status, and fertility. Our results also provide new insights into queen executions in the Argentine ant, a distinctive feature displayed by this species in its introduced range. Each spring, just before new sexuals appear, workers eliminate up to 90% of the mated queens in their colonies. We discovered that queens that survived execution had different CHC profiles from queens present before and during execution. More specifically, levels of some CHCs were higher in the survivors, suggesting that workers could eliminate queens based on their chemical profiles. In addition, queen CHC profiles differed based on season and species range (native vs. introduced). Overall, the results of this study provide new evidence that CHCs serve as queen signals and do more than just regulate worker reproduction.

Niche differentiation and fine-scale projections for Argentine ants based on remotely sensed data.

Modeling ecological niches of species is a promising approach for predicting the geographic potential of invasive species in new environments. Argentine ants (Linepithema humile) rank among the most successful invasive species: native to South America, they have invaded broad areas worldwide. Despite their widespread success, little is known about what makes an area susceptible--or not--to invasion. Here, we use a genetic algorithm approach to ecological niche modeling based on high-resolution remote-sensing data to examine the roles of niche similarity and difference in predicting invasions by this species. Our comparisons support a picture of general conservatism of the species' ecological characteristics, in spite of distinct geographic and community contexts.

Comparative transcriptomics reveals the conserved building blocks involved in parallel evolution of diverse phenotypic traits in ants.

BACKGROUND: Reproductive division of labor in eusocial insects is a striking example of a shared genetic background giving rise to alternative phenotypes, namely queen and worker castes. Queen and worker phenotypes play major roles in the evolution of eusocial insects. Their behavior, morphology and physiology underpin many ecologically relevant colony-level traits, which evolved in parallel in multiple species. RESULTS: Using queen and worker transcriptomic data from 16 ant species we tested the hypothesis that conserved sets of genes are involved in ant reproductive division of labor. We further hypothesized that such sets of genes should also be involved in the parallel evolution of other key traits. We applied weighted gene co-expression network analysis, which clusters co-expressed genes into modules, whose expression levels can be summarized by their 'eigengenes'. Eigengenes of most modules were correlated with phenotypic differentiation between queens and workers. Furthermore, eigengenes of some modules were correlated with repeated evolution of key phenotypes such as complete worker sterility, the number of queens per colony, and even invasiveness. Finally, connectivity and expression levels of genes within the co-expressed network were strongly associated with the strength of selection. Although caste-associated sets of genes evolve faster than non-caste-associated, we found no evidence for queen- or worker-associated co-expressed genes evolving faster than one another. CONCLUSIONS: These results identify conserved functionally important genomic units that likely serve as building blocks of phenotypic innovation, and allow the remarkable breadth of parallel evolution seen in ants, and possibly other eusocial insects as well.

Geographical potential of Argentine ants (Linepithema humile Mayr) in the face of global climate change.

Determining the spread and potential geographical distribution of invasive species is integral to making invasion biology a predictive science. We assembled a dataset of over 1000 occurrences of the Argentine ant (Linepithema humile), one of the world's worst invasive alien species. Native to central South America, Argentine ants are now found in many Mediterranean and subtropical climates around the world. We used this dataset to assess the species' potential geographical and ecological distribution, and to examine changes in its distributional potential associated with global climate change, using techniques for ecological niche modelling. Models developed were highly predictive of the species' overall range, including both the native distributional area and invaded areas worldwide. Despite its already widespread occurrence, L. humile has potential for further spread, with tropical coastal Africa and southeast Asia apparently vulnerable to invasion. Projecting ecological niche models onto four general circulation model scenarios of future (2050s) climates provided scenarios of the species' potential for distributional expansion with warming climates: generally, the species was predicted to retract its range in tropical regions, but to expand at higher latitude areas.

Strength in numbers: large and permanent colonies have higher queen oviposition rates in the invasive Argentine ant (Linepithema humile, Mayr).

Polydomy associated with unicoloniality is a common trait of invasive species. In the invasive Argentine ant, colonies are seasonally polydomous. Most follow a seasonal fission-fussion pattern: they disperse in the spring and summer and aggregate in the fall and winter. However, a small proportion of colonies do not migrate; instead, they inhabit permanent nesting sites. These colonies are large and highly polydomous. The aim of this study was to (1) search for differences in the fecundity of queens between mother colonies (large and permanent) and satellite colonies (small and temporal), (2) determine if queens in mother and satellite colonies have different diets to clarify if colony size influences social organization and queen feeding, and (3) examine if colony location relative to the invasion front results in differences in the queen's diet. Our results indicate that queens from mother nests are more fertile than queens from satellite nests and that colony location does not affect queen oviposition rate. Ovarian dissections suggest that differences in ovarian morphology are not responsible for the higher queen oviposition rate in mother vs. satellite nests, since there were no differences in the number and length of ovarioles in queens from the two types of colonies. In contrast, the higher δ(15)N values of queens from mother nests imply that greater carnivorous source intake accounts for the higher oviposition rates.

Mechanical defence in seeds to avoid predation by a granivorous ant.

Harvester ants have traditionally been considered as seed predators that negatively affect plants. In some cases, however, they can also act as positive seed dispersers. During field observations, we noted that a portion of Psoralea bituminosa seeds that were collected and carried to the nest by the granivorous harvester ant Messor barbarus were discarded intact in refuse piles outside the nest. We analyzed and compared the physical characteristics of size, mass and toughness in P. bituminosa seeds from two different origins: intact seeds found in the ant's refuse piles and seeds collected directly from the plants. Seeds from refuse piles were similar in width but lighter and tougher than seeds from the plant. Our results point to a mechanical defence based on seed toughness to avoid predation by M. barbarus and suggest that an elevated proportion (approximately 69%) of the seeds produced by P. bituminosa could be too tough to be consumed by this ant. These transported but uneaten seeds could benefit by being moved far from the mother plant and this could act as a selective evolutionary pressure towards tough seeds.

Ant behaviour and seed morphology: a missing link of myrmecochory.

Seed dispersal by ants (myrmecochory) is mediated by the presence of a lipid-rich appendage (elaiosome) on the seed that induces a variety of ants to collect the diaspores. When seeds mature or fall onto the ground, these ant species transport them to their nest. After eating the elaiosome, the seed is discarded in nest galleries or outside, in the midden or farther away, where seeds can potentially germinate. The final location of seeds with their elaiosomes removed was evaluated to assess the importance of possible handles (structures that ants can grasp to carry) in transporting ants during re-dispersal experiments of seeds from nests of six species of ants. The results indicate that seeds remained within the nest because the ants were not able to transport them out of the nest. As a consequence of the elaiosome being removed, small ant species could not take Euphorbia characias seeds out of their nests. Only large ant species could remove E. characias seeds from their nests. Attaching an artificial handle to E. characias seeds allowed small ant species to redistribute the seeds from their nests. On the other hand, Rhamnus alaternus seeds that have a natural handle after the elaiosome removal were removed from the nests by both groups of ant species. If a seed has an element that acts as a handle, it will eventually get taken out of the nest. The ants' size and their mandible gap can determine the outcome of the interaction (i.e. the pattern of the final seed shadow) and as a consequence, could influence the events that take place after the dispersal process.