Systematic reduction of natural enemies and competition across variable precipitation approximates buffelgrass invasiveness (Cenchrus ciliaris) in its native range.

Invasive grasses cause devastating losses to biodiversity and ecosystem function directly and indirectly by altering ecosystem processes. Escape from natural enemies, plant-plant competition, and variable resource availability provide frameworks for understanding invasion. However, we lack a clear understanding of how natural stressors interact in their native range to regulate invasiveness. In this study, we reduced diverse guilds of natural enemies and plant competitors of the highly invasive buffelgrass across a precipitation gradient throughout major climatic shifts in Laikipia, Kenya. To do this, we used a long-term ungulate exclosure experiment design across a precipitation gradient with nested treatments that (1) reduced plant competition through clipping, (2) reduced insects through systemic insecticide, and (3) reduced fungal associates through fungicide application. Additionally, we measured the interaction of ungulates on two stem-boring insect species feeding on buffelgrass. Finally, we measured a multiyear smut fungus outbreak. Our findings suggest that buffelgrass exhibits invasive qualities when released from a diverse group of natural stressors in its native range. We show natural enemies interact with precipitation to alter buffelgrass productivity patterns. In addition, interspecific plant competition decreased the basal area of buffelgrass, suggesting that biotic resistance mediates buffelgrass dominance in the home range. Surprisingly, systemic insecticides and fungicides did not impact buffelgrass production or reproduction, perhaps because other guilds filled the niche space in these highly diverse systems. For example, in the absence of ungulates, we showed an increase in host-specific stem-galling insects, where these insects compensated for reduced ungulate use. Finally, we documented a smut outbreak in 2020 and 2021, corresponding to highly variable precipitation patterns caused by a shifting Indian Ocean Dipole. In conclusion, we observed how reducing natural enemies and competitors and certain interactions increased properties related to buffelgrass invasiveness.

Global arthropod beta-diversity is spatially and temporally structured by latitude.

Global biodiversity gradients are generally expected to reflect greater species replacement closer to the equator. However, empirical validation of global biodiversity gradients largely relies on vertebrates, plants, and other less diverse taxa. Here we assess the temporal and spatial dynamics of global arthropod biodiversity dynamics using a beta-diversity framework. Sampling includes 129 sampling sites whereby malaise traps are deployed to monitor temporal changes in arthropod communities. Overall, we encountered more than 150,000 unique barcode index numbers (BINs) (i.e. species proxies). We assess between site differences in community diversity using beta-diversity and the partitioned components of species replacement and richness difference. Global total beta-diversity (dissimilarity) increases with decreasing latitude, greater spatial distance and greater temporal distance. Species replacement and richness difference patterns vary across biogeographic regions. Our findings support long-standing, general expectations of global biodiversity patterns. However, we also show that the underlying processes driving patterns may be regionally linked.

Comprehensive phylogeny of Pieridae butterflies reveals strong correlation between diversification and temperature.

Temperature is thought to be a key factor influencing global species richness patterns. We investigate the link between temperature and diversification in the butterfly family Pieridae by combining next generation DNA sequences and published molecular data with fine-grained distribution data. We sampled nearly 600 pierid butterfly species to infer the most comprehensive molecular phylogeny of the family and curated a distribution dataset of more than 800,000 occurrences. We found strong evidence that species in environments with more stable daily temperatures or cooler maximum temperatures in the warm seasons have higher speciation rates. Furthermore, speciation and extinction rates decreased in tandem with global temperatures through geological time, resulting in a constant net diversification.

Transposable Element Insertions Are Associated with Batesian Mimicry in the Pantropical Butterfly Hypolimnas misippus.

Hypolimnas misippus is a Batesian mimic of the toxic African Queen butterfly (Danaus chrysippus). Female H. misippus butterflies use two major wing patterning loci (M and A) to imitate three color morphs of D. chrysippus found in different regions of Africa. In this study, we examine the evolution of the M locus and identify it as an example of adaptive atavism. This phenomenon involves a morphological reversion to an ancestral character that results in an adaptive phenotype. We show that H. misippus has re-evolved an ancestral wing pattern present in other Hypolimnas species, repurposing it for Batesian mimicry of a D. chrysippus morph. Using haplotagging, a linked-read sequencing technology, and our new analytical tool, Wrath, we discover two large transposable element insertions located at the M locus and establish that these insertions are present in the dominant allele responsible for producing mimetic phenotype. By conducting a comparative analysis involving additional Hypolimnas species, we demonstrate that the dominant allele is derived. This suggests that, in the derived allele, the transposable elements disrupt a cis-regulatory element, leading to the reversion to an ancestral phenotype that is then utilized for Batesian mimicry of a distinct model, a different morph of D. chrysippus. Our findings present a compelling instance of convergent evolution and adaptive atavism, in which the same pattern element has independently evolved multiple times in Hypolimnas butterflies, repeatedly playing a role in Batesian mimicry of diverse model species.

A hydrogen isoscape for tracing the migration of herbivorous lepidopterans across the Afro-Palearctic range.

RATIONALE: Many insect species undertake multigenerational migrations in the Afro-tropical and Palearctic ranges, and understanding their migratory connectivity remains challenging due to their small size, short life span and large population sizes. Hydrogen isotopes (δ2 H) can be used to reconstruct the movement of dispersing or migrating insects, but applying δ2 H for provenance requires a robust isotope baseline map (i.e. isoscape) for the Afro-Palearctic. METHODS: We analyzed the δ2 H in the wings (δ2 Hwing ) of 142 resident butterflies from 56 sites across the Afro-Palearctic. The δ2 Hwing values were compared to the predicted local growing-season precipitation δ2 H values (δ2 HGSP ) using a linear regression model to develop an insect wing δ2 H isoscape. We used multivariate linear mixed models and high-resolution and time-specific remote sensing climate and environmental data to explore the controls of the residual δ2 Hwing variability. RESULTS: A strong linear relationship was found between δ2 Hwing and δ2 HGSP values (r2 = 0.53). The resulting isoscape showed strong patterns across the Palearctic but limited variation and high uncertainty for the Afro-tropics. Positive residuals of this relationship were correlated with dry conditions for the month preceding sampling whereas negative residuals were correlated with more wet days for the month preceding sampling. High intra-site δ2 Hwing variance was associated with lower relative humidity for the month preceding sampling and higher elevation. CONCLUSION: The δ2 Hwing isoscape is applicable for tracing herbivorous lepidopteran insects that migrate across the Afro-Palearctic range but has limited geolocation potential in the Afro-tropics. The spatial analysis of uncertainty using high-resolution climatic data demonstrated that many African regions with highly variable evaporation rates and relative humidity have δ2 Hwing values that are less related to δ2 HGSP values. Increasing geolocation precision will require new modeling approaches using more time-specific environmental data and/or independent geolocation tools.

Applying an evolutionary mismatch framework to understand disease susceptibility.

Noncommunicable diseases (NCDs) are on the rise worldwide. Obesity, cardiovascular disease, and type 2 diabetes are among a long list of "lifestyle" diseases that were rare throughout human history but are now common. The evolutionary mismatch hypothesis posits that humans evolved in environments that radically differ from those we currently experience; consequently, traits that were once advantageous may now be "mismatched" and disease causing. At the genetic level, this hypothesis predicts that loci with a history of selection will exhibit "genotype by environment" (GxE) interactions, with different health effects in "ancestral" versus "modern" environments. To identify such loci, we advocate for combining genomic tools in partnership with subsistence-level groups experiencing rapid lifestyle change. In these populations, comparisons of individuals falling on opposite extremes of the "matched" to "mismatched" spectrum are uniquely possible. More broadly, the work we propose will inform our understanding of environmental and genetic risk factors for NCDs across diverse ancestries and cultures.

Rapid radiation of ant parasitic butterflies during the Miocene aridification of Africa.

Africa has undergone a progressive aridification during the last 20 My that presumably impacted organisms and fostered the evolution of life history adaptations. We test the hypothesis that shift to living in ant nests and feeding on ant brood by larvae of phyto-predaceous Lepidochrysops butterflies was an adaptive response to the aridification of Africa that facilitated the subsequent radiation of butterflies in this genus. Using anchored hybrid enrichment we constructed a time-calibrated phylogeny for Lepidochrysops and its closest, non-parasitic relatives in the Euchrysops section (Poloyommatini). We estimated ancestral areas across the phylogeny with process-based biogeographical models and diversification rates relying on time-variable and clade-heterogeneous birth-death models. The Euchrysops section originated with the emerging Miombo woodlands about 22 million years ago (Mya) and spread to drier biomes as they became available in the late Miocene. The diversification of the non-parasitic lineages decreased as aridification intensified around 10 Mya, culminating in diversity decline. In contrast, the diversification of the phyto-predaceous Lepidochrysops lineage proceeded rapidly from about 6.5 Mya when this unusual life history likely first evolved. The Miombo woodlands were the cradle for diversification of the Euchrysops section, and our findings are consistent with the hypothesis that aridification during the Miocene selected for a phyto-predaceous life history in species of Lepidochrysops, with ant nests likely providing caterpillars a safe refuge from fire and a source of food when vegetation was scarce.

Non-invasive assessment of ovarian activity in free-ranging eastern black rhinoceros (Diceros bicornis michaeli) in Kenya.

Eastern black rhinos (Diceros bicornis michaeli) are a critically endangered species living in diverse habitats across Africa. In Kenya, once threatened with extinction due to massive poaching pressures, increased protection has resulted in losses being less than 1% annually today. Still, some populations have failed to achieve desired population growth targets. At Ol Jogi Wildlife Conservancy, some individuals are experiencing sub-optimal reproduction based on historical calving records and long inter-calving intervals (>3 years). Hormones drive the reproductive process, so non-invasive assessments of endocrine patterns can be useful indicators of individual reproductive health. In this study, we analysed longitudinal fecal progestagen metabolite (fPM) concentrations in all breeding female eastern black rhinos at Ol Jogi (n = 17) and compared the prevalence of irregular estrous cycles (longer or shorter than 20-40 days) and anestrous periods (interluteal period more than twice the length of a normal follicular phase, i.e. > 10 days) between optimal (inter-calving interval < 3 years) and sub-optimal (>3 years) reproducing individuals. Ten rhinos were pregnant during at least part of the study period. A total of 12 complete cycles were observed in seven females with an average length of 36 ± 3 days and equal numbers of regular and irregular cycles. Single anestrous periods averaging 67 ± 13 days were observed in five females. Surprisingly, a majority of cycles in optimal reproducing individuals were categorized as irregular based on fPM profiles. Overall, results suggest that irregular ovarian activity and isolated bouts of anestrus do not have negative impacts on reproductive performance in this subpopulation at Ol Jogi. A high priority is to continue using noninvasive hormone monitoring to evaluate how ecological or other variables influence reproductive success in this and other eastern black rhino subpopulations in Kenya.

The Afrotropical breeding grounds of the Palearctic-African migratory painted lady butterflies (Vanessa cardui).

Migratory insects are key players in ecosystem functioning and services, but their spatiotemporal distributions are typically poorly known. Ecological niche modeling (ENM) may be used to predict species seasonal distributions, but the resulting hypotheses should eventually be validated by field data. The painted lady butterfly (Vanessa cardui) performs multigenerational migrations between Europe and Africa and has become a model species for insect movement ecology. While the annual migration cycle of this species is well understood for Europe and northernmost Africa, it is still unknown where most individuals spend the winter. Through ENM, we previously predicted suitable breeding grounds in the subhumid regions near the tropics between November and February. In this work, we assess the suitability of these predictions through i) extensive field surveys and ii) two-year monitoring in six countries: a large-scale monitoring scheme to study butterfly migration in Africa. We document new breeding locations, year-round phenological information, and hostplant use. Field observations were nearly always predicted with high probability by the previous ENM, and monitoring demonstrated the influence of the precipitation seasonality regime on migratory phenology. Using the updated dataset, we built a refined ENM for the Palearctic-African range of V. cardui. We confirm the relevance of the Afrotropical region and document the missing natural history pieces of the longest migratory cycle described in butterflies.

Antimicrobial resistance patterns and characterisation of emerging beta-lactamase-producing Escherichia coli in camels sampled from Northern Kenya.

BACKGROUND: Animal husbandry practices in different livestock production systems and increased livestock-wildlife interactions are thought to be primary drivers of antimicrobial resistance (AMR) in Arid and Semi-Arid Lands (ASALs). Despite a tenfold increase in the camel population within the last decade, paired with widespread use of camel products, there is a lack of comprehensive information concerning beta-lactamase-producing Escherichia coli (E. coli) within these production systems. OBJECTIVES: Our study sought to establish an AMR profile and to identify and characterise emerging beta-lactamase-producing E. coli isolated from faecal samples obtained from camel herds in Northern Kenya. METHODS: The antimicrobial susceptibility profiles of E. coli isolates were established using the disk diffusion method, with beta-lactamase (bla) gene PCR product sequencing performed for phylogenetic grouping and genetic diversity assessments. RESULTS: Here we show, among the recovered E. coli isolates (n = 123), the highest level of resistance was observed for cefaclor at 28.5% of isolates, followed by cefotaxime at 16.3% and ampicillin at 9.7%. Moreover, extended-spectrum beta-lactamase (ESBL)-producing E. coli harbouring the blaCTX-M-15 or blaCTX-M-27 genes were detected in 3.3% of total samples, and are associated with phylogenetic groups B1, B2 and D. Multiple variants of non-ESBL blaTEM genes were detected, the majority of which were the blaTEM-1 and blaTEM-116 genes. CONCLUSIONS: Findings from this study shed light on the increased occurrence of ESBL- and non-ESBL-encoding gene variants in E. coli isolates with demonstrated multidrug resistant phenotypes. This study highlights the need for an expanded One Health approach to understanding AMR transmission dynamics, drivers of AMR development, and appropriate practices for antimicrobial stewardship in camel production systems within ASALs.

Evolutionary mismatch and the role of GxE interactions in human disease.

Globally, we are witnessing the rise of complex, non-communicable diseases (NCDs) related to changes in our daily environments. Obesity, asthma, cardiovascular disease, and type 2 diabetes are part of a long list of "lifestyle" diseases that were rare throughout human history but are now common. A key idea from anthropology and evolutionary biology-the evolutionary mismatch hypothesis-seeks to explain this phenomenon. It posits that humans evolved in environments that radically differ from the ones experienced by most people today, and thus traits that were advantageous in past environments may now be "mismatched" and disease-causing. This hypothesis is, at its core, a genetic one: it predicts that loci with a history of selection will exhibit "genotype by environment" (GxE) interactions and have differential health effects in ancestral versus modern environments. Here, we discuss how this concept could be leveraged to uncover the genetic architecture of NCDs in a principled way. Specifically, we advocate for partnering with small-scale, subsistence-level groups that are currently transitioning from environments that are arguably more "matched" with their recent evolutionary history to those that are more "mismatched". These populations provide diverse genetic backgrounds as well as the needed levels and types of environmental variation necessary for mapping GxE interactions in an explicit mismatch framework. Such work would make important contributions to our understanding of environmental and genetic risk factors for NCDs across diverse ancestries and sociocultural contexts.

Global biogeography of warning coloration in the butterfly Danaus chrysippus.

Warning coloration provides a textbook example of natural selection, but the frequent observation of polymorphism in aposematic species presents an evolutionary puzzle. We investigated biogeography and polymorphism of warning patterns in the widespread butterfly Danaus chrysippus using records from citizen science (n = 5467), museums (n = 8864) and fieldwork (n = 2586). We find that polymorphism in three traits controlled by known mendelian loci is extensive. Broad allele frequency clines, hundreds of kilometres wide, suggest a balance between long-range dispersal and predation of unfamiliar morphs. Mismatched clines for the white hindwing and forewing tip in East Africa are consistent with a previous finding that the black wingtip allele has spread recently in the region through hitchhiking with a heritable endosymbiont. Light/dark background coloration shows more extensive polymorphism. The darker genotype is more common in cooler regions, possibly reflecting a trade-off between thermoregulation and predator warning. Overall, our findings show how studying local adaptation at the global scale provides a more complete picture of the evolutionary forces involved.

Stepwise evolution of a butterfly supergene via duplication and inversion.

Supergenes maintain adaptive clusters of alleles in the face of genetic mixing. Although usually attributed to inversions, supergenes can be complex, and reconstructing the precise processes that led to recombination suppression and their timing is challenging. We investigated the origin of the BC supergene, which controls variation in warning coloration in the African monarch butterfly, Danaus chrysippus. By generating chromosome-scale assemblies for all three alleles, we identified multiple structural differences. Most strikingly, we find that a region of more than 1 million bp underwent several segmental duplications at least 7.5 Ma. The resulting duplicated fragments appear to have triggered four inversions in surrounding parts of the chromosome, resulting in stepwise growth of the region of suppressed recombination. Phylogenies for the inversions are incongruent with the species tree and suggest that structural polymorphisms have persisted for at least 4.1 Myr. In addition to the role of duplications in triggering inversions, our results suggest a previously undescribed mechanism of recombination suppression through independent losses of divergent duplicated tracts. Overall, our findings add support for a stepwise model of supergene evolution involving a variety of structural changes. This article is part of the theme issue 'Genomic architecture of supergenes: causes and evolutionary consequences'.

Detection of Antibodies to Ehrlichia spp. in Dromedary Camels and Co-Grazing Sheep in Northern Kenya Using an Ehrlichia ruminantium Polyclonal Competitive ELISA.

A disease with clinical and post-mortem presentation similar to those seen in heartwater, a tick-borne disease of domestic and wild ruminants caused by the intracellular bacterium Ehrlichia ruminantium, was first reported in dromedary camels in Kenya in 2016; investigations carried out at the time to determine the cause were inconclusive. In the present study, we screened sera from Kenyan camels collected before (2015) and after (2020) the 2016 disease outbreak for antibodies to Ehrlichia spp. using an E. ruminantium polyclonal competitive ELISA (PC-ELISA). Median antibody levels were significantly higher (p < 0.0001) amongst camels originating from areas where the heartwater-like disease was reported than from disease-free areas, for animals sampled in both 2015 and 2020. Overall median seropositivity was higher in camels sampled in 2015 than in 2020, which could have been due to higher mean age in the former group. Camels that were PCR-positive for Candidatus Ehrlichia regneryi had significantly lower (p = 0.03) median antibody levels than PCR-negative camels. Our results indicate that Kenyan camels are frequently exposed to E. ruminantium from an early age, E. ruminantium was unlikely to have been the sole cause of the outbreak of heartwater-like disease; and Ca. E. regneryi does not appreciably cross-react with E. ruminantium in the PC-ELISA.

Strengthening global health security by improving disease surveillance in remote rural areas of low-income and middle-income countries.

The COVID-19 pandemic has underscored the need to strengthen national surveillance systems to protect a globally connected world. In low-income and middle-income countries, zoonotic disease surveillance has advanced considerably in the past two decades. However, surveillance efforts often prioritise urban and adjacent rural communities. Communities in remote rural areas have had far less support despite having routine exposure to zoonotic diseases due to frequent contact with domestic and wild animals, and restricted access to health care. Limited disease surveillance in remote rural areas is a crucial gap in global health security. Although this point has been made in the past, practical solutions on how to implement surveillance efficiently in these resource-limited and logistically challenging settings have yet to be discussed. We highlight why investing in disease surveillance in remote rural areas of low-income and middle-income countries will benefit the global community and review current approaches. Using semi-arid regions in Kenya as a case study, we provide a practical approach by which surveillance in remote rural areas can be strengthened and integrated into existing systems. This Viewpoint represents a transition from simply highlighting the need for a more holistic approach to disease surveillance to a solid plan for how this outcome might be achieved.

Evidence of nutrient translocation in response to smoke exposure by the East African ant acacia, Vachellia drepanolobium.

Fire is a major selective force on arid grassland communities, favoring traits such as the smoke-induced seed germination response seen in a wide variety of plant species. However, little is known about the relevance of smoke as a cue for plants beyond the seedling stage.We exposed a fire-adapted savanna tree, Vachellia (=Acacia) drepanolobium, to smoke and compared nutrient concentrations in leaf and root tissues to unexposed controls. Experiments were performed on three age cohorts: 2-year-old, 9-month-old, and 3-month-old plants.For the 2-year-old plants exposed to smoke, carbon and nitrogen concentrations were lower in the leaves and higher in the roots than controls. Less pronounced trends were found for boron and magnesium.In contrast, smoke-exposed 3-month-old plants had lower root nitrogen concentrations than controls. No significant differences were found in the 9-month-old plants, and no significant shifts in other nutrient concentrations were observed between plant tissues for any of the three age cohorts. Synthesis: Our findings are consistent with smoke-induced translocation of nutrients from leaves to roots in 2-year-old V. drepanolobium. This could represent a novel form of fire adaptation, with variation over the course of plant development. The translocation differences between age cohorts highlight the need to investigate smoke response in older plants of other species. Accounting for this adaptation could better inform our understanding of savanna community structure and nutrient flows under fire regimes altered by anthropogenic land use and climate change.

Genome assembly of Danaus chrysippus and comparison with the Monarch Danaus plexippus.

Milkweed butterflies in the genus Danaus are studied in a diverse range of research fields including the neurobiology of migration, biochemistry of plant detoxification, host-parasite interactions, evolution of sex chromosomes, and speciation. We have assembled a nearly chromosomal genome for Danaus chrysippus (known as the African Monarch, African Queen, and Plain Tiger) using long-read sequencing data. This species is of particular interest for the study of genome structural change and its consequences for evolution. Comparison with the genome of the North American Monarch Danaus plexippus reveals generally strong synteny but highlights 3 inversion differences. The 3 chromosomes involved were previously found to carry peaks of intraspecific differentiation in D. chrysippus in Africa, suggesting that these inversions may be polymorphic and associated with local adaptation. The D. chrysippus genome is over 40% larger than that of D. plexippus, and nearly all of the additional ∼100 Megabases of DNA comprises repeats. Future comparative genomic studies within this genus will shed light on the evolution of genome architecture.

Draft genome sequences of three emerging beta-lactamase-producing Escherichia coli in the camel production system in Northern Kenya.

We report the draft genome sequences and annotation of three beta-lactamase-producing Escherichia coli ( E.coli) strains isolated from fecal samples of healthy camels in Laikipia county, Kenya. This data adds to the online genome resources to support the ongoing antimicrobial resistance surveillance in the livestock-wildlife interface.

Socioeconomic status effects on health vary between rural and urban Turkana.

BACKGROUND AND OBJECTIVES: Understanding the social determinants of health is a major goal in evolutionary biology and human health research. Low socioeconomic status (often operationalized as absolute material wealth) is consistently associated with chronic stress, poor health and premature death in high-income countries. However, the degree to which wealth gradients in health are universal-or are instead made even steeper under contemporary, post-industrial conditions-remains poorly understood. METHODOLOGY: We quantified absolute material wealth and several health outcomes among a population of traditional pastoralists, the Turkana of northwest Kenya, who are currently transitioning toward a more urban, market-integrated lifestyle. We assessed whether wealth associations with health differed in subsistence-level versus urban contexts. We also explored the causes and consequences of wealth-health associations by measuring serum cortisol, potential sociobehavioral mediators in early life and adulthood, and adult reproductive success (number of surviving offspring). RESULTS: Higher socioeconomic status and greater material wealth predicts better self-reported health and more offspring in traditional pastoralist Turkana, but worse cardiometabolic health and fewer offspring in urban Turkana. We do not find robust evidence for either direct biological mediators (cortisol) or indirect sociobehavioral mediators (e.g. adult diet or health behaviors, early life experiences) of wealth-health relationships in either context. CONCLUSIONS AND IMPLICATIONS: While social gradients in health are well-established in humans and animals across a variety of socioecological contexts, we show that the relationship between wealth and health can vary within a single population. Our findings emphasize that changes in economic and societal circumstances may directly alter how, why and under what conditions socioeconomic status predicts health. LAY SUMMARY: High socioeconomic status predicts better health and more offspring in traditional Turkana pastoralists, but worse health and fewer offspring in individuals of the same group living in urban areas. Together, our study shows that under different economic and societal circumstances, wealth effects on health may manifest in very different ways.