APRIL 30, 2019

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www.pnas.org/cgi/doi/10.1073/iti1819116 PNAS | April 30, 2019 | vol. 116 | no. 18 | 8635–8637

Suicide-bombing aphids defend colonies against predators

The tendency of social insects, such as ants, termites, and aphids, to engage in self-sacrificing acts of altruism for the benefit of colonies has long been considered one of nature’s oddities. Mayako Kutsukake et al. (pp. 8950–8959) describe the biochemical underpinnings of a form of self-destructive defense mounted by the social aphid Nipponaphis monzeni when predators attack the aphid’s colonies, which are housed in galls on winter hazel trees. In the spring, when lepi-dopteran insects dig into the galls in search of food, dozens of aphid soldiers scurry toward the wound and expel lipid- rich body fluids. In a risky operation that can shut them out of the gall or smother them outright, the rapidly shriveling soldiers briskly plaster the wound with the milky body fluids, which coagulate and close the wound. Biochemical analysis of the fluid revealed a potent clot-forming mix: an abun-dance of previously undescribed, large, globular, lipid-laden cells that resemble hemocytes; the amino acid tyrosine; the enzyme phenoloxidase, which converts tyrosine to melanin in a stepwise pathway; and a repeat-containing protein, which is woven into the clot’s latticework. Thus, the synchronized expulsion of lipid-rich fluid by aphid soldiers creates a soft clot around the gall wound that is swiftly hardened and melanin- darkened through the action of phenoloxidase. While such wound healing in individual N. monzeni represents an unre-markable form of innate immunity triggered by predators, the soldiers’ collective action is an amplified immune response marshaled for social defense. According to the authors, the study uncovers molecular clues to the evolutionary roots of altruistic social defense. — P.N.

Early agricultural strategies in southern Polynesia

The importance of the tropical crop taro during the early human colonization of New Zealand and other southern Polynesian islands is poorly understood. Little evidence of cultivation of the crop remains, in contrast to evidence of big-game hunting and later expansion of sweet potato crops. Matthew Prebble et al. (pp. 8824–8833) collected sediment cores from three southern Polynesian islands: Ahuahu, Raivavae, and Rapa. The cores, contain-ing fossil plants and animal remains, extend past the initial colonization period beginning in the 13th century CE. The results suggest a history of taro

production in the islands, given that taro pollen appeared in the fossil records during 1300–1550 CE. The presence of pollen indicates flowering plants, which would be absent if the plants had been frequently harvested. During early cultiva-tion, fire was likely used to clear forest cover, as suggested by sedimentary charcoal. Fire decreased over time, concurrent with an increase in short-lived plants, including weeds and leaf vegetables indica-tive of high-intensity production, forest decline, and species extinctions leading to widespread sweet potato cultivation by 1500 CE. According to the authors, the results show how Neolithic societies coped with the spread of tropical crops into mar-ginal habitats. — P.G.

Soldier nymphs of N. monzeni repairing a gall breach by discharging body fluid.

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Antigay bias and legalizing same-sex marriages Social norms can influence behaviors and attitudes, but it is unclear how local legislation may influ-ence citizens’ attitudes. To examine how state-level legalization of gay marriage influenced antigay bias in the United States, Eugene Ofosu et al. (pp. 8846–8851) geolocated 949,664 respondents who completed surveys between 2005 and 2016 that measured implicit and explicit antigay bias through Project Implicit. In addition to analyzing antigay bias among self-reported heterosexuals and individuals who did not report their sexuality, the authors also examined nationally representative data from the American National Election Studies dataset, which included 10,870 respondents, from 2008, 2012, and 2016. In all samples, both implicit and explicit antigay bias decreased over time across the United States in states that legalized gay marriage. Bias decreased at almost double the rate in states that enacted state-level legalization, compared with states that did not enact local legalization. However, in states that did not locally pass legalization, anti-gay bias increased following federal legalization. The effects were consistent across all models. The findings suggest that legislation locality may moder-ate the biases of local residents, and that legislation and attitudes may reinforce each other, according to the authors. — M.S.

Location-specific air pollution damages Fine particulate matter (PM2.5) is a major cause of premature mortality in the United States. The health impacts of air pollution depend on location. Andrew Goodkind et al. (pp. 8775–8780) developed

a model to calculate location-specific damages due to primary PM2.5 and PM2.5 precursor emissions. Applying the model to the US Environmental Pro-tection Agency 2011 National Emissions Inven-tory revealed considerable variability in damages per ton emitted by location, with the most harmful 10% of emissions responsible for nearly half of the total damages. The authors estimated 107,000 total cases of premature death in the United States due to anthropogenic PM2.5 in 2011, with a societal cost of $886 billion. Emissions associated with energy consumption contributed to more than half of the damages. One-third of damages occurred within 8 km of the emissions source, whereas one-quarter of the damages occurred more than 256 km from the source, suggesting that both local and long- distance impacts contribute significantly to the over-all impacts. According to the authors, the results highlight the importance of modeling emissions at fine spatial scales and could help prioritize emissions mitigation efforts. — B.D.

Secondary protein structure drives toxicity in Alzheimer’s diseaseIn Alzheimer’s disease (AD), cognitive impairment and disease progression are associated with the aggregation of amyloid-beta (Aβ) peptides into toxic, soluble oligomers. However, clinical trials for AD have not targeted Aβ oligomers, and a mech-anistic explanation for the role of the Aβ peptide in AD remains elusive. Dylan Shea et al. (pp. 8895–8900) report that Aβ soluble oligomers adopt a non-standard structure called the α-sheet, which forms early in Aβ aggregation and is strongly associated with cell toxicity. The authors designed α-sheet pep-tides that specifically and tightly bind the toxic Aβ oligomers, inhibiting Aβ aggregation by up to 96% and reducing toxicity in nerve cells, whereas control peptides had no significant effect. In a mouse model of AD, intracranial injection of the α-sheet peptides into the right hemisphere of the brain reduced toxic, soluble Aβ oligomers by up to 40% 24 hours later, compared with the untreated left hemisphere. In a nematode worm model, exposure to α-sheet pep-tides delayed the onset of Aβ-induced paralysis, whereas the control peptide had no effect. Accord-ing to the authors, the findings could lead to the development of diagnostic and therapeutic strate-gies for AD and other amyloid diseases. — J.W.

Selective inhibition of peanut-specific antibodies Allergen protein binding to allergen-specific IgE antibodies triggers potentially fatal reactions, such as peanut allergies. Peter Deak et al. (pp. 8966–8974) developed a nanoparticle-based assay to screen parts of allergenic peanut proteins, or

8636 | www.pnas.org/cgi/doi/10.1073/iti1819116 In this issue

Industrial air pollution. Image courtesy of Wikimedia Commons/Alfred T. Palmer.

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www.pnas.org/cgi/doi/10.1073/iti1819116 PNAS | April 30, 2019 | vol. 116 | no. 18 | 8637

epitopes, against IgE antibodies from 16 patients with peanut allergy. The authors identified two epi-topes capable of eliciting strong allergic reactions in serum samples from all or nearly all patients. The authors engineered molecules called covalent het-erobivalent inhibitors (cHBIs), designed to selec-tively and irreversibly bind to IgEs that recognize these two epitopes, thus permanently preventing the IgEs from binding to peanut proteins and trig-gering allergic reactions. The cHBIs bound to IgE in serum from allergic patients more strongly than in control serum, and prevented allergen binding to patient IgE in vitro. Treatment with cHBIs inhibited more than 80% of the allergic response to crude peanut extract in serum samples from 14 of 16 patients, and significantly reduced basophil activa-tion in whole blood from three individual patients. The results suggest that cHBIs could form the basis of a therapeutic approach to allergies, according to the authors. — B.D.

Covalent inhibitor binding to antigen binding site (red) and secondary binding site (orange) of antibody (blue) and bonding with antibody (black).

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