Search bioRxiv⌕ Search

Biology subjects

Economo, E. P.

Publications and source records attributed to Economo, E. P..

At least 19 recordsLinked to original sources

Spiders as natural DNA samplers recover arthropod community diversity and biotic interactions across space and time

Global arthropod decline demands effective biodiversity monitoring strategies. However, most current monitoring approaches do not provide an exhaustive picture of arthropod community structure. In particular, biotic interactions and temporal patterns of biodiversity change are still poorly understood. Here we explore the possibility of addressing these two shortfalls using spiders, one of the most important predators of terrestrial arthropods, as natural samplers for arthropod community DNA. We conducted several experiments comparing the recovered community composition between spider gut contents and traditional monitoring methods. Additionally, we used archived spiders from long-term collections to assess the preservation of prey DNA over time. Spiders proved to be highly efficient natural DNA samplers, with gut content metabarcoding revealing similar community composition and alpha- and beta-diversity like traditional methods. Unique arthropod taxa were detected by spider gut contents and traditional methods respectively, indicating that these two approaches can serve as valuable complements to each other. Well-preserved archived spiders effectively reconstructed historical diets up to 20 years back in time, showing that historical spider collections can act as time capsules of the wider diversity that occurred in the spider's habitat. Spiders as natural samplers overcome critical shortfalls in biodiversity monitoring and contribute to our future understanding of community assembly across space and time.

ecology↗

Varroa mites escape the evolutionary trap of haplodiploidy

Genetic diversity is essential for populations adapting to environmental-changes. Following genetic bottlenecks, invasive species often have reduced diversity, yet must rapidly adapt to novel environments. This paradox is especially pronounced in parasites, which face repeated transmission bottlenecks and anthropogenic countermeasures. The challenge of maintaining diversity in the short-term intensifies in haplodiploid species, where males inherit and transmit only half of their mothers genome, limiting effective population size. To examine how such species may maintain adaptability, we studied inheritance in Varroa mites (Varroa destructor), globally invasive honey bee parasite. Using three-generation pedigrees, we found that Varroa is not haplodiploid, as previously thought. Rather, females produce diploid sons who transmit either maternal allele to daughters. This system slows reduced heterozygosity loss under sib-mating, compared to ancestral haplodiploidy, increasing effective population size and adaptability. Our findings reveal a rare reversion from haplodiploidy, long considered an evolutionary end state, and suggest reproductive plasticity underlies the resilience of invasive parasites like Varroa.

evolutionary biology↗

A new leaf sensing organ in a predatory insect group, the praying mantises (Mantodea)

Animals sensory systems enable them to navigate and interact with their environments. Adaptive specializations of these systems can generate novel structures or organs that support highly unique niche adaptations. We report the discovery of a novel sensory organ in a group of praying mantises (Insecta, Mantodea, Nanomantoidea), which have an unusual "leaf-planking" ecomorphic life strategy, laying against the undersides of broadleaf vegetation. Histology, scanning electron microscopy, and x-ray computed tomography all support the novelty of this distinct morphology while electrophysiology reveals that the sensory organ, herein designated the gustifolium organ, detects plant volatiles. The location of the gustifolium organon the ventral thoracic surface of these mantises appears to facilitate the chemical detection of the leaves on which it resides. The gustifolium is a novel plant volatile-detecting sensory structure in an obligate predatory insect, directly linked to a newly-identified, highly-adapted life strategy.

zoology↗

Generalized mutualisms promote range expansion in both plant and ant partners

Mutualism improves organismal fitness, but strong dependence on another species can also limit a species ability to thrive in a new range if its partner is absent. We assembled a large, global dataset on mutualistic traits and species ranges to investigate how multiple plant-animal and plant-microbe mutualisms affect the spread of legumes and ants to novel ranges. We found that generalized mutualisms increase the likelihood that a species establishes and thrives beyond its native range, whereas specialized mutualisms either do not affect or reduce non-native spread. This pattern held in both legumes and ants, indicating that specificity between mutualistic partners is a key determinant of ecological success in a new habitat. Our global analysis shows that mutualism plays an important, if often overlooked, role in plant and insect invasions.

ecology↗

Parallel and divergent morphological adaptations underlying the evolution of jumping ability in ants

Jumping is a rapid locomotory mode widespread in terrestrial organisms. However, it is a rare specialization in ants. Forward jumping has been reported within four distantly related ant genera: Gigantiops, Harpegnathos, Myrmecia, and Odontomachus. The temporal engagement of legs/body parts during jump, however, varies across these genera. It is unknown what morphological adaptations underlie such behaviors, and whether jumping in ants is solely driven directly by muscle contraction or additionally relies on elastic recoil mechanism. We investigate the morphological adaptations for jumping behavior by comparing differences in the locomotory musculature between jumping and non-jumping relatives using x-ray micro- CT and 3D morphometrics. We found that the size-specific volumes of the trochanter depressor muscle (scm6) of the middle and hind legs are 3-5 times larger in jumping ants, and that one coxal remotor muscle (scm2) is reduced in volume in the middle and/or hind legs. Notably, the enlargement in the volume of other muscle groups is directly linked to the legs or body parts engaged during the jump. Furthermore, a direct comparison of the muscle architecture revealed two significant differences between in jumping versus non-jumping ants: First, the relative Physiological Cross-Sectional Area (PCSA) of the trochanter depressor muscles of all three legs were larger in jumping ants, except in the front legs of O. rixosus and M. nigrocincta; second, the relative muscle fiber length was shorter in jumping ants compared to non-jumping counterparts, except in the front legs of O. rixosus and M. nigrocincta. This suggests that the difference in relative muscle volume in jumping ants is largely invested in the area (PCSA), and not in fiber length. There was no clear difference in the pennation angle between jumping and non-jumping ants. However, the length of hind legs relative to body length was longer in jumping ants. Based on direct comparison of the observed vs. possible work and power output during jumps, we surmise that direct muscle contractions suffice to explain jumping performance, in two species, but elastic recoil is likely important in one. We suggest that increased investment in jumping-relevant musculature is a primary morphological adaptation that separates jumping from non-jumping ants. These results elucidate the common and idiosyncratic morphological changes underlying this rare adaptation in ants.

evolutionary biology↗

Behavioural individuality determines infection risk in clonal ant colonies

In social groups, disease risk is not distributed evenly across group members. Individual behaviour is a key source of variation in infection risk, yet its effects are difficult to separate from those of other factors. Here, we combine long-term epidemiological experiments and automated tracking in clonal raider ant colonies, where behavioural individuality emerges among identical workers. We find that: 1) division of labour determines the distribution of parasitic nematodes (Diploscapter) among hosts, showing that differences in infection can emerge from behavioural variation alone, 2) infections affect colony social organisation by causing infected workers to stay in the nest. By disproportionally infecting some workers and shifting their spatial distribution, infections reduce division of labour and increase spatial overlap between hosts, which is expected to facilitate parasite transmission. Thus, division of labour, a defining feature of many societies, not only shapes infection risk and distribution but can also be modified by parasites.

animal behavior and cognition↗

Breakdown in seasonal dynamics of ant communities with land-cover change

Concerns about widespread human-induced declines in insect populations are mounting, yet little is known about how land-use change modifies the dynamics of insect communities, particularly in understudied biomes. Here, we examine how the seasonal patterns of ant activity--key drivers of terrestrial ecosystem functioning--vary with human-induced land cover change on a subtropical island landscape. Using trap captures sampled biweekly from a biodiversity monitoring network covering Okinawa Island, Japan, we processed 1.2 million individuals and reconstructed activity patterns within and across habitat types. Forest communities exhibited greater variability than those in more developed areas. Using time-series decomposition to deconstruct this pattern, we found that ant communities at sites with greater human development exhibited diminished seasonality, reduced synchrony, and higher stochasticity compared to those at sites with greater forest cover. Our results cannot be explained by variation in either regional or in situ temperature patterns, or by differences in species richness or composition among sites. We conclude that the breakdown of natural seasonal patterns of functionally key insect communities may comprise an important and underappreciated consequence of global environmental change that must be better understood across Earths biomes.

ecology↗

Habitat degradation homogenizes ecological responses to typhoons across a subtropical island

Climate change is increasing the frequency, intensity, and duration of extreme weather events across the globe. Understanding the capacity for ecological communities to withstand and recover from such events is critical. Typhoons are extreme weather events that are expected to broadly homogenise ecological dynamics through structural damage to vegetation and longer-term effects of salinization. Given their unpredictable nature, monitoring ecological responses to typhoons is challenging, particularly for mobile animals such as birds. Here, we report spatially variable ecological responses to typhoons across terrestrial landscapes. Using a high temporal resolution passive acoustic monitoring network across 24 sites on the subtropical island of Okinawa, Japan, we found that typhoons elicit divergent ecological responses among Okinawas diverse terrestrial habitats, as indicated by increased spatial variability of biological sound production (biophony) and individual species detections. This suggests that soniferous communities are capable of a diversity of different responses to typhoons. That is, spatial insurance effects among local ecological communities provide resilience to typhoons at the landscape scale. Even though site-level typhoon impacts on soundscapes and bird detections were not particularly strong, monitoring at scale with high temporal resolution across a broad spatial extent nevertheless enabled detection of spatial heterogeneity in typhoon responses. Further, species-level responses mirrored those of acoustic indices, underscoring the utility of such indices for revealing insight into fundamental questions concerning disturbance and stability. Our findings demonstrate the significant potential of landscape-scale acoustic sensor networks to capture the understudied ecological impacts of unpredictable extreme weather events.

ecology↗

Incorporating sampling bias into permutation tests for niche and distribution models

Randomization tests are often used with species niche and distribution models to estimate model performance, test hypotheses, and measure methodological biases. Many of these tests involve building null models representing the hypothesis that there is no association between the species occurrences and the environmental predictors, then comparing the empirical model to null distributions built from these models. These null models are commonly based on points randomly selected with a uniform probability from the study area. However, spatial sampling bias, a near-universal feature of the occurrence data used to build niche and distribution models, results in a non-uniform probability of observing species in different areas even when species occurrences are unrelated to environmental predictors. Failing to account for this bias in randomization tests results in null distributions that do not accurately represent the null hypothesis, potentially leading to incorrect conclusions. In this study, we use simulations to demonstrate that uniform sampling in randomization tests can lead to unacceptable rates of type I error and poor estimates of methodological bias when spatial sampling bias is present in the occurrence data. We present a new method that incorporates a bias estimate into replicate simulations for these randomization tests, and show that this adjustment can reduce type I error rates to an acceptable level.

ecology↗

Climate and ant richness explain the global distribution of ant-plant mutualisms

Biotic interactions are known to play an important role in shaping species geographic distributions and diversity patterns. However, the role of mutualistic interactions in shaping global diversity patterns remains poorly quantified, particularly with respect to interactions with invertebrates. Moreover, it is unclear how the nature of different mutualisms interacts with abiotic drivers and affects diversity patterns of mutualistic organisms. Here, we present a global-scale biogeographic analysis of three different ant-plant mutualisms, differentiating between plants bearing domatia, extrafloral nectaries (EFNs), and elaiosomes, based on comprehensive geographic distributions of [~]15,000 flowering plants and [~]13,000 ant species. Domatia and extrafloral nectaries involve indirect plant defenses provided by ants, while elaiosomes attract ants to disperse seeds. Our results show distinct biogeographic patterns of different ant-plant mutualisms, with domatium- and EFN-bearing plant richness decreasing sharply from the equator towards the poles, while elaiosome-bearing plants prevail at mid-latitudes. Contemporary climate, especially mean annual temperature and precipitation, emerge as the most important predictor of ant-associated plant diversity. In hot and moist regions, typically the tropics, domatium- and EFN-bearing plant richness increases with related ant guild richness, while in warm regions plants with elaiosomes are strongly linked to interacting ants. Our results suggest that ant richness in combination with climate drives the spatial variation of plants bearing domatia, extrafloral nectaries, and elaiosomes, highlighting the importance of mutualistic interactions for understanding plant biogeography and its response to global change.

ecology↗

Periodic Environmental Disturbance Drives Repeated Ecomorphological Diversification in an Adaptive Radiation of Antarctic Fishes

The ecological theory of adaptive radiation has profoundly shaped our conceptualization of the rules that govern diversification. However, while many radiations follow classic early burst patterns of diversification as they fill ecological space, the longer-term fates of these radiations depend on many factors, such as climatic stability. In systems with periodic disturbances, species-rich clades can contain nested adaptive radiations of subclades with their own distinct diversification histories, and how adaptive radiation theory applies in these cases is less clear. Here, we investigated patterns of ecological and phenotypic diversification within two iterative adaptive radiations of cryonotothenioid fishes in Antarcticas Southern Ocean: crocodile icefishes and notoperches. For both clades, we observe evidence of repeated diversification into disparate regions of trait space between closely related taxa and into overlapping regions of trait space between distantly related taxa. We additionally find little evidence that patterns of ecological divergence are correlated with evolution of morphological disparity, suggesting that these axes of divergence may not be tightly linked. Finally, we reveal evidence of repeated convergence in sympatry that suggests niche complementarity. These findings reflect the dynamic history of Antarctic marine habitats, and may guide hypotheses of diversification dynamics in environments characterized by periodic disturbance.

evolutionary biology↗

New distribution data and phylogenetic approach reveal bioregionalization of the western Palearctic ants

AimBiogeographic regionalization has fascinated biogeographers and ecologists for centuries and is endued with new vitality by evolutionary perspectives. However, progress is scant for most insect groups due to shortfalls in distribution and phylogenetic information, namely Wallacean and Darwinian shortfalls respectively. Here, we used the western Palearctic ants as the case to tackle these shortfalls and test their biogeographic structure through novel distribution data and phylogenetic approaches. LocationWestern Palearctic realm. TaxonAnts (Formicidae). MethodsFirstly, we developed a refined database integrating the occurrences of 747 ant species across 207 regions of the western Palearctic realm, based on newly expert-validated records derived from the existing global ant biodiversity informatics. Using range estimates for these species derived from polygons and species distribution modelling, we produced species assemblages in 50 x 50 km grid cells. We calculated taxonomic and phylogenetic turnover of ant assemblages, performing hierarchical clustering analysis using the Simpson dissimilarity index to delineate biogeographic structure. ResultsAt both the regional list- and grid assemblage-levels, the Mediterranean has higher turnover and more biogeographic regions than northern Europe, both taxonomically and phylogenetically. Delineations based on grid assemblages detected more detailed biogeographic transitions, while those based on regional lists showed stronger insularity in biogeographic structure. The phylogenetic regionalization suggested closer but varied affinities between assemblages in comparison to the taxonomic approach. Main conclusionsHere, we integrated expert-validated regional lists, species distribution modelling, and a recent phylogeny to tackle Wallacean and Darwinian shortfalls for an important insect group by developing a next-generation map of biogeographic regionalization for the western Palearctic ants. The results of this study suggest strong constraints from geographic barriers and potential effects of climatic history on ant distributions and evolutionary history, and also provide baseline spatial information for future investigations of regional insect distributions.

zoology↗

Global determinants of the distribution of insect genetic diversity

Understanding global patterns of genetic diversity (GD) is essential for describing, monitoring, and preserving life on Earth. To date, efforts to map macrogenetic patterns have been restricted to vertebrates, which comprise only a small fraction of Earths biodiversity. Here, we construct the first global map of predicted insect mitochondrial (COI) GD, derived from publicly available data. We calculate the mitochondrial GD mean (GDM) and evenness (GDE) of insect assemblages across the globe, identify their environmental correlates, and make predictions of mitochondrial GD levels in unsampled areas based on environmental data. Using the largest single-locus genetic dataset yet assembled, we find that mitochondrial GDE follows a quadratic latitudinal gradient peaking in the subtropics. Both mitochondrial GDM and GDE positively correlate with seasonally hot temperatures, as well as climate stability since the last glacial maximum. Our models explain 27.9% and 24.0% of the observed variation in mitochondrial GDM and GDE in insects, respectively, making an important step towards understanding global biodiversity patterns in the most diverse animal taxon.

evolutionary biology↗

The global spread and invasion capacities of alien ants

The ecological and economic impacts of biological invasions are usually highly conspicuous, but these are the outcome of a global, multistage process that is obscured from view. For most taxa, we lack a large-scale picture of the movements of alien species, the biases and barriers that promote or inhibit their spread at each stage, and blind spots in our ability to detect species during their spread. For instance, countries rely heavily on customs interceptions to prevent new species introductions, but their efficacy for detecting invaders remains unclear. To address these gaps, we synthesize and provide data at unprecedented geographic resolution on the global diversity and distribution of alien ants, a pervasive group strongly impacting humans and ecosystems. From >145,000 records spanning 602 regions, we identify 522 ant species exhibiting human-mediated spread, doubling recent estimates of their diversity. We show that movements of alien ant species across regions globally are non-random and, moreover, that these flows differ by the extents to which species invade--ranging from arrival to indoor establishment, naturalization, and harmful status. Importantly, we find that almost two-thirds of the 309 species that naturalize globally--most of which are ground- and litter-dwelling--are absent from customs interceptions, which record disproportionately high numbers of arboreal species. Our results illustrate the vast, yet uneven extent of ant invasions globally, and suggest that most alien species bypass biosecurity controls while spreading successfully worldwide. This raises doubts on the efficacy of current customs interceptions procedures and highlights a need for radically new approaches. Significance statementBiological invasions impact humans and ecosystems tremendously. Invasions are difficult to address because little is known about large-scale patterns of spread, species capacities to invade ecosystems, and the efficacy of existing biosecurity measures. This paper tackles these issues for alien ants, one of the most damaging groups of invasive animals. An unprecedented dataset reveals that 522 ant species exhibit human-mediated spread, 270 more than previously known. Species are grouped under four levels of invasion capacity corresponding to different invasion barriers. Geographic sources and sinks for the groups differ globally. Two-thirds of species with naturalization capacity have never been recorded at customs interceptions, which fail to detect many litter-dwelling species. Novel detection and control strategies for inconspicuous alien organisms are needed.

ecology↗

Automated segmentation of insect anatomy from micro-CT images using deep learning

Three-dimensional (3D) imaging, such as micro-computed tomography (micro-CT), is increasingly being used by organismal biologists for precise and comprehensive anatomical characterization. However, the segmentation of anatomical structures remains a bottleneck in research, often requiring tedious manual work. Here, we propose a pipeline for the fully-automated segmentation of anatomical structures in micro-CT images utilizing state-of-the-art deep learning methods, selecting the ant brain as a test case. We implemented the U-Net architecture for 2D image segmentation for our convolutional neural network (CNN), combined with pixel-island detection. For training and validation of the network, we assembled a dataset of semi-manually segmented brain images of 94 ant species. The trained network predicted the brain area in ant images fast and accurately; its performance tested on validation sets showed good agreement between the prediction and the target, scoring 80% Intersection over Union (IoU) and 90% Dice Coefficient (F1) accuracy. While manual segmentation usually takes many hours for each brain, the trained network takes only a few minutes. Furthermore, our network is generalizable for segmenting the whole neural system in full-body scans, and works in tests on distantly related and morphologically divergent insects (e.g., fruit flies). The latter suggest that methods like the one presented here generally apply across diverse taxa. Our method makes the construction of segmented maps and the morphological quantification of different species more efficient and scalable to large datasets, a step toward a big data approach to organismal anatomy.

evolutionary biology↗

Mandibular morphology, task specialization, and bite mechanics in Pheidole ants (Hymenoptera: Formicidae)

The remarkable ecological and evolutionary success of ants was associated with the evolution of reproductive division of labor, in which sterile workers perform most colony tasks whereas reproductives become specialized in reproduction. In some lineages, the worker force became further subdivided into morphologically distinct subcastes (e.g. minor vs. major workers), allowing for the differential performance of particular roles in the colony. However, the functional and ecological significance of morphological differences between subcastes is not well understood. Here, we applied Finite Element Analysis (FEA) to explore the functional differences between major and minor ant worker mandibles. Analyses were carried out on mandibles of two Pheidole species, a dimorphic ant genus. In particular, we test whether major mandibles evolved to minimize stress when compared to minors using combinations of tooth and masticatory margin bites under strike and pressure conditions. Majors performed better in pressure conditions yet, contrary to our expectations, minors performed better in strike bite scenarios. Moreover, we demonstrate that even small morphological differences in ant mandibles might lead to substantial differences in biomechanical responses to bite loading. These results also underscore the potential of FEA to uncover biomechanical consequences of morphological differences within and between ant worker castes.

ecology↗

Genomic signature of shifts in selection in a sub-alpine ant and its physiological adaptations

Understanding how organisms adapt to extreme environments is fundamental and can provide insightful case studies for both evolutionary biology and climate-change biology. Here, we take advantage of the vast diversity of lifestyles in ants to identify genomic signatures of adaptation to extreme habitats such as high altitude. We hypothesised two parallel patterns would occur in a genome adapting to an extreme habitat: i) strong positive selection on genes related to adaptation and, ii) a relaxation of previous purifying selection. We tested this hypothesis by sequencing the high-elevation specialist Tetramorium alpestre and four other phylogenetic related species. In support of our hypothesis, we recorded a strong shift of selective forces in T. alpestre, in particular a stronger magnitude of diversifying and relaxed selection when compared to all other ants. We further disentangled candidate molecular adaptations in both gene expression and protein-coding sequence that were identified by our genome-wide analyses. In particular, we demonstrate that T. alpestre has i) a derived level of expression for stv and other heat-shock proteins in chill shock tests, and ii) enzymatic enhancement of Hex-T1, a rate-limiting regulatory enzyme that controls the entry of glucose into the glycolytic pathway. Together, our analyses highlight the adaptive molecular changes that support colonisation of high-altitude environments.

evolutionary biology↗

Macroevolutionary integration of phenotypes within and across ant worker castes

Phenotypic traits are often integrated into evolutionary modules: sets of organismal parts that evolve together. In social insect colonies the concepts of integration and modularity apply to sets of traits both within and among functionally and phenotypically differentiated castes. On macroevolutionary timescales, patterns of integration and modularity within and across castes can be clues to the selective and ecological factors shaping their evolution and diversification. We develop a set of hypotheses describing contrasting patterns of worker integration and apply this framework in a broad (246 species) comparative analysis of major and minor worker evolution in the hyperdiverse ant genus Pheidole. Using geometric morphometrics in a phylogenetic framework, we inferred fast and tightly integrated evolution of mesosoma shape between major and minor workers, but slower and more independent evolution of head shape between the two worker castes. Thus, Pheidole workers are evolving as a mixture of intra- and inter-caste integration and rate heterogeneity. The decoupling of homologous traits across worker castes may represent an important process facilitating the rise of social complexity.

evolutionary biology↗