Human introductions of plant species often lead to secondary invasions by non-native insects or range expansions of native ones. For instance, native insects may undergo extralimital spread when they adopt non-native plants that are closely related to their native host plants. Leptocoris soapberry bugs feeding on plants in the soapberry family (Sapindaceae) provide prime examples of such host shifts. In Australia and South Africa, the introduction of non-native sapindaceous plants, as well as human-mediated changes in the distributions of native ones, has the potential to impact the ecology and evolutionary dynamics of native soapberry bugs. Observations indicated that, in both countries, the ranges of some native Leptocoris species have expanded substantially due to the human-mediated movement and introduction of native and non-native sapindaceous species. In Australia, the native L. rufomarginatus has established in the Sydney region, where native Alectryon species have been introduced and naturalised well outside their historical ranges, i.e., extralimital host plant species, and the introduced non-native L. vicinus was found to be localised at its initial introduction site in Darwin on the non-native Schleichera oleosa. Species distribution models showed that vast areas in Australia currently have a suitable climate for both the native and non-native host plants of soapberry bugs. This suggests that range expansions by these host plants and insects are likely to continue. In South Africa, the native L. mutilatus now occurs ~1,000 km beyond its previously described range, feeding on the invasive balloon vine Cardiospermum grandiflorum and the non-native Australian tree A. connatus. Evidence is provided for differentiation in the proboscis length of L. mutilatus insects feeding on different non-native, invasive, and native host plants. In Australia, the native L. tagalicus was also successfully hybridised and backcrossed with the non-native L. vicinus, providing the first report of interspecific hybridisation for soapberry bugs under laboratory conditions. The shared evolutionary history between soapberry bugs and sapindaceous host plants suggests that further changes in these insects’ distributions and adaptive responses to novel host plants are likely to occur. Taken together, these results demonstrate how human-mediated plant dispersal affect the ecology, distribution, and evolution of native insects.
The successful management of invasive alien species is hampered when they share habitats with native congeners. However, in some instances, the status of resident congeners (as alien or native) in the invaded range is unknown, further complicating management efforts. Here, we investigate the genetic relationships between Cardiospermum balloon vine species, focussing on C. grandiflorum and C. halicacabum, to better understand the introduction histories of these species and the status of C. halicacabum in Australia. Cardiospermum grandiflorum is considered to be an invasive species in the country while the status of C. halicacabum is debated. Based on network and phylogenetic analyses of chloroplast and nuclear gene sequencing data, respectively, we infer an alien status for C. halicacabum in Australia and show that multiple introductions likely founded invasive populations of both balloon vine species in the country. We discuss our findings in the light of the management of balloon vines in Australia, with an emphasis on biological control.
Native species can evolve rapidly in response to utilising invasive species as novel resources. We investigated the genetic and trait differentiation of the Australian soapberry bug Leptocoris tagalicus across three biotypes: those feeding on invasive Cardiospermum grandiflorum in New South Wales (NSW) and Queensland (Qld), invasive C. halicacabum in the Northern Territory (NT), and on the native host Alectryon tomentosus (in Qld). Genetic analyses revealed moderate differentiation between NT insects and those from NSW and Qld (F ST = 0.033). Conversely, insects from NSW and Qld had low genetic differentiation, irrespective of their host plant associations (F ST = 0.008). Field data and data from a multi-generation experiment indicated ongoing adaptation in proboscis length in insects feeding on the two invasive host plant species, likely in response to the sizes of their fruits. Multi-generation hybridisation experiments demonstrated high narrow sense heritability in insect proboscis length and body size (H2 = 0.48 and 0.4, respectively). Crosses involving F1 hybrids of insect biotypes generally outperformed inter-biotype and control crosses. Taken together, these findings support ongoing genetic differentiation among L. tagalicus biotypes across different spatial scales, even in instances of high gene flow.
Pollinating seed predators are partners in a specialized plant-insect mutualism where insects pollinate the flower ovules of the seeds that they later consume. Such relationships have proven rare but provide a unique perspective on the mechanisms that drive (co)evolution. We combine natural history and community science observations to identify the red-shouldered bug (Jadera haematoloma) as the first member of the insect order Hemiptera to be classified in this guild. We use laboratory- and field-based experiments to demonstrate that J. haematoloma are consuming nectar and providing a pollination service for their host plants. However, the pollination benefit to the host is later reduced by seed predation from the pollinator's offspring. Furthermore, this study expands our perspective on the diet breadth of J. haematoloma, which is a model system for rapid ecological adaptation of feeding morphology that was historically attributed solely to selective pressures associated with accessing the seeds inside the fruit of their host plant.
Introduced predators are thought to be responsible for the decline and extinction of their native prey. The prey naivety hypothesis provides a mechanism for these declines, suggesting that native prey are vulnerable to introduced predators as their coevolutionary history is insufficiently long for antipredator behaviours to fully develop. The prey naivety hypothesis thus predicts that prey will be less responsive to introduced predators than to native predators. Australia's endemic small mammals are thought to be vulnerable to predation by red foxes because they are less responsive to – or naive of – a predator with whom they have only co‐occurred since the 19th century. To test whether nativeness determines antipredator behaviours we compared small mammal behavioural responses to fox scent outside (Australia) and inside the foxes' native range (North America and Israel). We conducted giving‐up density experiments in the deserts of these three regions and evaluated small mammal antipredator responses to fox scent. To place these results in a broader context, we then integrated our results into a global meta‐analysis of studies assessing prey responsiveness to fox scent. All small mammals similarly increased their vigilance in response to fox scent, regardless of their coevolutionary history with foxes. Australian small mammals responded with greater wariness to fox scent, by decreasing time at food patches in response to fox scent more than Israeli and American small mammals did. However, we found no evidence that this behaviour influenced foraging as nut consumption was unaffected. Our meta‐analysis revealed that globally, small mammals respond with similar wariness to fox scent regardless of whether foxes are their native predator. We found no evidence that Australian small mammals respond in a maladaptive manner, compared to the foxes' native prey. Our results suggest that animals can develop antipredator behaviours to introduced predators to the same magnitude as native prey.
Predicting future evolutionary change is a critical challenge in the Anthropocene as geographic range shifts and local extinction emerge as hallmarks of planetary change. Hence, spatial sorting-a driver of rapid evolution in which dispersal-associated traits accumulate along expanding range edges and within recolonized habitats-might be of growing importance in ecology and conservation. We report on the results of a natural experiment that monitored recolonization of host plants by the seed-feeding, red-shouldered soapberry bug, Jadera haematoloma, after local extinctions from catastrophic flooding in an extreme hurricane. We tested the contribution of spatial sorting to generate rapid and persistent evolution in dispersal traits, as well as in feeding traits unrelated to dispersal. Long-winged dispersal forms accumulated in recolonized habitats and due to genetic correlation, mouthparts also became longer and this shift persisted across generations. Those longer mouthparts were probably adaptive on one host plant species but maladaptive on two others based on matching the optimum depth of seeds within their host fruits. Moreover, spatial sorting eroded recently evolved adaptive divergence in mouthpart length among all host-associated biotypes, an outcome pointing to profound practical consequences of the extreme weather event for local adaptation, population resilience and evolutionary futures.
The prey naivety hypothesis posits that prey are vulnerable to introduced predators because many generations in slow gradual coevolution are needed for appropriate avoidance responses to develop. It predicts that prey will be more responsive to native than introduced predators and less responsive to introduced predators that differ substantially from native predators and from those newly established. To test these predictions, we conducted a global meta-analysis of studies that measured the wariness responses of small mammals to the scent of sympatric mammalian mesopredators. We identified 26 studies that met our selection criteria. These studies comprised 134 experiments reporting on the responses of 36 small mammal species to the scent of six introduced mesopredators and 12 native mesopredators. For each introduced mesopredator, we measured their phylogenetic and functional distance to local native mesopredators and the number of years sympatric with their prey. We used predator and prey body mass as a measure of predation risk. Globally, small mammals were similarly wary of the scent of native and introduced mesopredators; phylogenetic and functional distance between introduced mesopredators and closest native mesopredators had no effect on wariness; and wariness was unrelated to the number of prey generations, or years, since first contact with introduced mesopredators. Small mammal wariness was associated with predator-prey body mass ratio, regardless of the nativity. The one thing animals do not seem to recognize is whether their predators are native.
Host races represent an important step in the speciation process of phytophagous insects as they reflect the maintenance of genetically divergent host‐associated populations in the face of appreciable gene flow. The red‐shouldered soapberry bug, Jadera haematoloma (Herrich‐Schäffer) (Hemiptera: Rhopalidae), is an oligophagous seed predator with a history of host race evolution on plant associations in the (soapberry) family Sapindaceae. Soapberry bugs are a model group for understanding rapid ecological adaptation to their hosts, and hence good candidates for investigating evolutionary divergence in host associations over short timescales. Here, we describe the recent discovery of Mexican buckeye, Ungnadia speciosa Endl., as a host of J. haematoloma in a region of the Chihuahuan desert including west Texas and southeastern New Mexico, USA. This host differs from J. haematoloma ’s previously recorded hosts in the Sapindaceae in seed chemistry, ecology, and phylogeny. The tendency toward rapid, host‐associated adaptations by populations of J. haematoloma and the unique biology of the newly discovered Ungnadia host create the opportunity for potential host race formation, as it overlaps geographically with two previously recorded host plants in this region – the native western soapberry tree, Sapindus saponaria var. drummondii (Hook & Arn.), and the non‐native goldenrain tree, Koelreuteria paniculata Laxm. We explore the possibility of host race formation on Ungnadia ‐associated insects by testing for host‐associated differentiation in morphology and feeding behaviors. We find evidence of differentiation in the length of the mouth parts, which is an ecologically relevant feeding trait between host plant species with larger or smaller seed capsules. This divergence is maintained in the face of potential gene flow by reproductive isolation in the form of habitat isolation, which we detect in host preference trials. Together, our results demonstrate that soapberry bugs associated with this newly discovered host exhibit morphological and behavioral traits consistent with host race formation, but additional work is required to confirm its state along the speciation continuum.
People have literally had skin in the game from the beginning of arthropod repellent science more than a century ago. However, formal ethical guidance for human subject repellent studies appeared much more recently, as regulatory agencies that require human data have adopted biomedical standards. The 2005 US EPA Human Studies Rule inaugurated a modern chapter in arthropod repellent development, in which the augmented demands at the intersection of scientific rigor and subject protection have escalated study costs and added challenging strategic quandaries to the pursuit of improved repellents. Risk concerns have likewise led to reliance on carbon dioxide trap counts rather than human subjects for area repellent studies and have fueled a move toward arm-in-cage studies to replace field testing in the European Union. However, neither traps nor arm-in-cage tests necessarily replicate human subject field outcomes, suggesting that uncritical regulatory reliance on surrogate hosts and laboratory systems may risk data relevance while also hampering the development of products that perform better under actual conditions of use. Other repellent modalities, like treated fabrics, will also benefit from methods that more clearly show modes of action and protection from pathogens. While the modern regulatory environment has likely slowed development of new repellent products, efforts toward harmonization among regulatory agencies may increase efficiencies and expedite international commercialization. The coalescence of a more advanced regulatory platform may facilitate the development of new technologies for personal-use protection from arthropods, with better linkages to integrated public health management of disease transmission and pesticide resistance.
Michael Paul Nelson , ∗ Chelsea Batavia , Kate J. Brandis, Scott P. Carroll, Danielle Celermajer, Wayne Linklater, Erick Lundgren, Daniel Ramp, Jamie Steer, Esty Yanco, and Arian D. Wallach 8 Department of Forest Ecosystems and Society, Oregon State University, 321 Richardson Hall, Corvallis, OR, 97331, U.S.A. Centre for Ecosystem Science, School of Biological, Environmental and Earth Science, University of New South Wales, Sydney, NSW, 2052, Australia Department of Entomology & Nematology, University of California Davis, 1 Shield Avenue, Davis, CA, 95616, U.S.A. Department of Sociology and Social Policy, Faculty of Arts and Social Sciences, The University of Sydney, Camperdown, NSW, 2006, Australia Department of Environmental Studies, California State University – Sacramento, 6000 J Street, Amador Hall, 555D, Sacramento, CA, 95819, U.S.A. Centre for Biodiversity & Restoration Ecology, Victoria University of Wellington, Wellington, 6021, New Zealand Centre for African Conservation Ecology, Nelson Mandela University, Port Elizabeth, 6019, South Africa Centre for Compassionate Conservation, Faculty of Science, University of Technology Sydney, Ultimo, NSW, 2007, Australia Biodiversity Department, Greater Wellington Regional Council, Wellington, 6142, New Zealand
Michael Paul Nelson , ∗ Chelsea Batavia , Kate J. Brandis, Scott P. Carroll, Danielle Celermajer, Wayne Linklater, Erick Lundgren, Daniel Ramp, Jamie Steer, Esty Yanco, and Arian D. Wallach 8 Department of Forest Ecosystems and Society, Oregon State University, 321 Richardson Hall, Corvallis, OR, 97331, U.S.A. Centre for Ecosystem Science, School of Biological, Environmental and Earth Science, University of New South Wales, Sydney, NSW, 2052, Australia Department of Entomology & Nematology, University of California Davis, 1 Shield Avenue, Davis, CA, 95616, U.S.A. Department of Sociology and Social Policy, Faculty of Arts and Social Sciences, The University of Sydney, Camperdown, NSW, 2006, Australia Department of Environmental Studies, California State University – Sacramento, 6000 J Street, Amador Hall, 555D, Sacramento, CA, 95819, U.S.A. Centre for Biodiversity & Restoration Ecology, Victoria University of Wellington, Wellington, 6021, New Zealand Centre for African Conservation Ecology, Nelson Mandela University, Port Elizabeth, 6019, South Africa Centre for Compassionate Conservation, Faculty of Science, University of Technology Sydney, Ultimo, NSW, 2007, Australia Biodiversity Department, Greater Wellington Regional Council, Wellington, 6142, New Zealand
Large-bodied mammalian herbivores dominated Earth’s terrestrial ecosystems for several million years before undergoing substantial extinctions and declines during the Late Pleistocene (LP) due to prehistoric human impacts. The decline of large herbivores led to widespread ecological changes due to the loss of their ecological functions, as driven by their unique combinations of traits. However, recently, humans have significantly increased herbivore species richness through introductions in many parts of the world, potentially counteracting LP losses. Here, we assessed the extent to which for renewed research on introduced herbivore ecologies in light of paleoecological change and suggest that shifting focus from eradication to landscape and predator protection may have broader biodiversity benefits.
Conservation science involves the collection and analysis of data. These scientific practices emerge from values that shape who and what is counted. Currently, conservation data are filtered through a value system that considers native life the only appropriate subject of conservation concern. We examined how trends in species richness, distribution, and threats change when all wildlife count by adding so‐called non‐native and feral populations to the International Union for Conservation of Nature Red List and local species richness assessments. We focused on vertebrate populations with founding members taken into and out of Australia by humans (i.e., migrants). We identified 87 immigrant and 47 emigrant vertebrate species. Formal conservation accounts underestimated global ranges by an average of 30% for immigrants and 7% for emigrants; immigrations surpassed extinctions in Australia by 52 species; migrants were disproportionately threatened (33% of immigrants and 29% of emigrants were threatened or decreasing in their native ranges); and incorporating migrant populations into risk assessments reduced global threat statuses for 15 of 18 species. Australian policies defined most immigrants as pests (76%), and conservation was the most commonly stated motivation for targeting these species in killing programs (37% of immigrants). Inclusive biodiversity data open space for dialogue on the ethical and empirical assumptions underlying conservation science.
Transgenic crops that produce insecticidal proteins from Bacillus thuringiensis (Bt) can suppress pests and reduce insecticide sprays, but their efficacy is reduced when pests evolve resistance. Although farmers plant refuges of non-Bt host plants to delay pest resistance, this tactic has not been sufficient against the western corn rootworm, Diabrotica virgifera virgifera. In the United States, some populations of this devastating pest have rapidly evolved practical resistance to Cry3 toxins and Cry34/35Ab, the only Bt toxins in commercially available corn that kill rootworms. Here, we analyzed data from 2011 to 2016 on Bt corn fields producing Cry3Bb alone that were severely damaged by this pest in 25 cropreporting districts of Illinois, Iowa, and Minnesota. The annual mean frequency of these problem fields was 29 fields (range 7 to 70) per million acres of Cry3Bb corn in 2011 to 2013, with a cost of $163 to $227 per damaged acre. The frequency of problem fields declined by 92% in 2014 to 2016 relative to 2011 to 2013 and was negatively associated with rotation of corn with soybean. The effectiveness of corn rotation for mitigating Bt resistance problems did not differ significantly between crop-reporting districts with versus without prevalent rotation-resistant rootworm populations. In some analyses, the frequency of problem fields was positively associated with planting of Cry3 corn and negatively associated with planting of Bt corn producing both a Cry3 toxin and Cry34/35Ab. The results highlight the central role of crop rotation for mitigating impacts of D. v. virgifera resistance to Bt corn.
Significance Humans have caused extinctions of large-bodied mammalian herbivores over the past ∼100,000 y, leading to cascading changes in ecosystems. Conversely, introductions of herbivores have, in part, numerically compensated for extinction losses. However, the net outcome of the twin anthropogenic forces of extinction and introduction on herbivore assemblages has remained unknown. We found that a primary outcome of introductions has been the reintroduction of key ecological functions, making herbivore assemblages with nonnative species more similar to preextinction ones than native-only assemblages are. Our findings support calls for renewed research on introduced herbivore ecologies in light of paleoecological change and suggest that shifting focus from eradication to landscape and predator protection may have broader biodiversity benefits.
The Anthropocene biosphere constitutes an unprecedented phase in the evolution of life on Earth with one species, humans, exerting extensive control. The increasing intensity of anthropogenic forces in the twenty-first century has widespread implications for attempts to govern both human-dominated ecosystems and the last remaining wild ecosystems. Here, we review how evolutionary biology can inform governance and policies in the Anthropocene, focusing on five governance challenges that span biodiversity, environmental management, food and other biomass production, and human health. The five challenges are: ( a) evolutionary feedbacks, ( b) maintaining resilience, ( c) alleviating constraints, ( d) coevolutionary disruption, and ( e) biotechnology. Strategies for governing these dynamics will themselves have to be coevolutionary, as eco-evolutionary and social dynamics change in response to each other.
Following their establishment in new communities, invasive species may cause evolutionary changes in resident native species. This is clearly true for phytophagous insects, which may adapt rapidly when utilising abundant and widespread introduced hosts. The balloon vines Cardiospermumhalicacabum and C.grandiflorum were introduced to South Africa approximately 100 years ago and are classified as minor and major weeds, respectively. Here we assess the potential evolutionary impact of these vines on native Leptocoris soapberry bug populations in Kruger National Park (KNP), using phylogenetic and morphometric analyses. We found that soapberry bugs associated with C.halicacabum are genetically and morphologically distinct from those associated with C.grandiflorum. This suggests that native soapberry bugs in KNP exhibit some degree of host preference, indicating that these vines may have had significant evolutionary consequences for these insects. The proboscis length of soapberry bugs feeding on C.halicacabum closely matched fruit size, often being longer than fruit size at the population level. These soapberry bugs are therefore well-suited to feeding on this introduced plant species.