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Six-legged success stories
Current Biology
Magazine Feature
Six-legged success stories Insects represent the majority of today’s animal biodiversity, although many of their species are now at risk from land-use change and pesticides. Given their vast number of species, it is no wonder that science is still busy finding new connections in their ecology and evolution, including in the ways they co-evolve with plants and other organisms. Michael Gross reports. Life on Earth, from our anthropocentric perspective, is often described as the evolution towards ‘higher’, more intelligent life forms including primates and then ourselves as the alleged pinnacle of creation. Alien visitors passing through the Solar System might first spot the green vegetation and measure its oxygen output. But anybody looking at species diversity, varieties of successful ecological strategies, and sheer number of individual animals would come to the conclusion that over the last 400 million years Earth has become the planet of the insects. There are more than a million described species in the class of insects (Ectognatha), which together with the less expansive Entognatha (around 5,000 species) comprise the Hexapods, or everything that has six legs. They outnumber all other species known to science, such that any project aiming to account for all eukaryotic species, like the Earth BioGenome Project (Curr. Biol. (2018) 28, R719– R721), will have to spend most of its time with insects. Research has uncovered a number of factors that have contributed to their spectacular success, as Michael Engel from the University of Kansas at Lawrence, USA, has explained in this journal (Curr. Biol. (2015) 25, R868– R872). Firstly, they suffered surprisingly few losses at higher phylogenetic levels during the last mass extinction — the one that defined the end of the Cretaceous and wiped out the non-avian dinosaurs among many other species. Thus, while much of the biodiversity we see around us, including birds and mammals, had only around 66 million years to diversify, insects go back more than 410 million years. In this timeframe, Engel reports, there have been several synergistic factors that enabled explosive growth of some groups at later points, without
triggering it directly. These include the first ever invention of flight, soon after the arthropod ancestors came out of the oceans, then, at a later point, complete metamorphosis, which led to the Holometabola groups now comprising more than 80% of insect diversity. Combined with an especially flexible development and the robust and versatile body plan based on the arthropod exoskeleton, these traits enabled insects to shape their world (Curr. Biol. (2017) 27, R283–R285) and interact with many other species in many different ways. Ants and plants In the Early Cretaceous (146–100 million years ago), flowering plants (angiosperms) spread around the world and pollinating insects have played an important part in this. Much of the current concern about population declines in insects is motivated by the
loss of pollinators that may ultimately threaten our food provision (Curr. Biol. (2018) 28, R1121–R1123). Over the same timescale, another kind of interaction evolved between many kinds of plants and many species of ants, where plants provide food and shelter, and ants offer defence and seed dispersal. They even protect plants from diseases (Oikos (2019) https://doi.org/10.1111/oik.06744). Research has shown that mutualism between ants (family of Formicidae, with more than 12,000 named species) and plants has enhanced diversification of plants, but its impact on the ants has been less clear-cut. Matthew Nelsen and colleagues at the Field Museum of Natural History at Chicago, USA, have addressed this question by analysing relevant traits in phylogenies covering more than 10,000 plant genera and 1,730 species of ants (Proc. Natl. Acad. Sci. USA (2018) 115, 12253–12258). Their results suggest a sequential series of events rather than a simultaneous boost for both sides. Ancestral ant species were carnivores nesting and foraging on the ground. Foraging on plants was the first relevant change, followed by accepting and looking for plant food. Omnivorous ants started to feed on plant sap and possibly on the honeydew produced by aphids (Curr. Biol. (2019) 29, R1–R3).
Plant like: Insects have adapted to many different forms and functions, including the striking camouflage of stick and leaf insects. The photo shows a giant prickly stick insect (Extatosoma tiaratum), a species endemic to Australia. (Photo: sandid/Pixabay.)
Current Biology 29, R1105–R1121, November 4, 2019
R1105
Current Biology
Magazine order that extend from Africa through to New Zealand. Appearances proved deceptive on the island of Madagascar as well. “The flamboyant stick insects of Madagascar, for instance, descended from a single ancestral species that colonised the island approximately 45 million years ago,” explains Sarah Banks from the group of Sven Bradler at the University of Göttingen. The oldest lineages of stick insects lead back to the time after the last mass extinction, 66 million years ago. This finding suggests that the characteristic camouflage evolved in response to the rapidly growing threat of birds and mammals taking over after the dinosaurs.
Green habitat: Acacias grow hollow spines (domatia), which ants use as shelter. (Photo: Ryan Somma/Flickr (CC BY-SA 2.0).)
Plant structures beneficial for ants only evolved later. These include extrafloral nectaries secreting nectar on stems or leaves: elaiosomes, which are food packages enticing ants to carry seeds with them, and domatia, hollow structures in which ants can nest, such as the spines formed by some species of acacias. These adaptations enabling ants to become fully engaged in a plant-based niche largely evolved in the Cenozoic, that is after the last mass extinction. Thus, the authors describe a stepwise increase in mutual dependence. During this tightening of the relations, the plants showed enhanced diversification rates, but the ants did not. In an effort to expand these studies to a wider range of species, Katrina Kaur and colleagues at the University of Toronto, Canada, have used text mining of more than 89,000 published abstracts to capture published traits associated with ant–plant mutualism (PLoS Comput. Biol. (2019) 15, e1007323). Like Nelsen and colleagues, their analysis suggests that ants diversified before becoming engaged in mutualistic relations with plants. “To our surprise, the intimate and often beneficial relationships that ants have with plants apparently did not help to generate the over 14,000 ant species on Earth today,” Kaur said. “Mutualism R1106
may put the brakes on the rise of new species or increase the threat of extinction because an ant’s fate becomes linked to its plant partner’s.” Leaves and sticks While ants developed many ways of living with and on plants, the group of leaf and stick insects (order Phasmatodea) evolved sophisticated ways of resembling plants in an effort not to be detected by predators hunting by vision. A relatively recent radiation has led to more than 3,000 species that may be very diverse visually, but are hard to sort into a phylogenetic tree based on existing sequence data. Therefore, the deeper connections of their evolutionary history have remained controversial. In a new study, Sabrina Simon from Wageningen University and Research, The Netherlands, and other researchers from around the world have analysed 27 new transcriptomes of Phasmatodea in combination with previously published sequence information (Front. Ecol. Evol. (2019) 7, 345). For each species, more than 2,000 separate genes were analysed. The results contradict some of the earlier divisions made on the basis of appearances. Instead, the new phylogenetic tree has a strong geographic division into western (New World) and eastern members of the
Current Biology 29, R1105–R1121, November 4, 2019
Termites and other cockroaches Insect orders have been shaken up and redefined in the last few decades as molecular studies forced revision of classifications based on anatomy and behaviour. As recently as 2007, molecular research confirmed that termites are just a eusocial group of cockroaches. While this relationship had been suspected since the early 20th century, it was not reflected in traditional systematics. Losing their status as a separate order, the termites were merged into the order Blattodea, which now includes around 4,400 species of cockroaches as well as more than 3,000 species of termites. Many of these species play important roles as degraders of dead wood, which also makes them noticeable players in the global carbon cycle and thus in climate regulation. Some termitederived enzymes are also of interest for the production of biofuel from otherwise indigestible biomaterials. Some Blattodea are also considered pests, and termites in particular can endanger wooden structures in some areas. Thus, there are many ecological and economical reasons to better understand their biology. Dominic Evangelista from the Sorbonne at Paris, France, and colleagues have recently presented a new, detailed phylogenetic analysis based on 2,370 protein-coding genes from 66 species representing all but one of the major groups of Blattodea (Proc. R. Soc. B (2019) 286, 20182076). “The analysis confirmed the new affiliation of termites within the cockroaches and clarified some
Current Biology
Magazine long-standing problems, including the relatively young age of the order,” says Sabrina Simon, who was a senior author of this study as well as the one on stick insects. While previous work had suggested origins some 240–180 million years ago, long before fossil evidence can be linked to it, the new study suggests that most major groups of Blattodea arose during the Cretaceous (147–66 million years ago), which is more easily reconciled with the fossil record. It also proves that any fossils resembling cockroaches in the Carboniferous (359–299 million years ago) can be safely excluded. Social behaviours like maternal brood care are not ancestral features of the group, the researchers find. Instead, they suggest that the common ancestor packaged its eggs in a protective parcel, the ootheca, and buried this in a hole, as many cockroaches still do today. This behaviour may also explain the evolution of wood-degrading behaviour, the authors say, concluding: “We suggest that the transition from a freeliving ancestor to living within wood (in Cryptocercus and termites) could have been partially driven by advantages gained in protection of the ootheca.” Zooming in on termites, and on the group of Termitidae in particular, Ales Bucek and Thomas Bourguignon from the Okinawa Institute of Science and Technology Graduate University, Japan, describe the origins of termite fungiculture elsewhere in this issue of Current Biology (https://doi.org/10.1016/j. cub.2019.08.076). The termite subfamily Macrotermitinae produces comb-like structures in its hives where they cultivate fungal symbionts. This, the authors find, is a derived feature probably unrelated to the earlier loss of protozoan symbionts in the termite gut. Origins of flight Some of the orders of insects have been a challenge to systematics, but the very root of the insects’ family tree poses even bigger and more fundamental questions. Key events here are the very first invention of flight in animals, which separated the Pterygota (winged insects) from the likes of silverfishes (order Zygentoma) and bristletails (order Archaeognatha). Early flying insects had stiff wings set at a fixed angle like today’s mayflies, damselflies and dragonflies. The
Social cockroaches: Termites are economically important for their ability to degrade wood. The evolution of this trait may be related to the habit of closely related cockroaches to bury their eggs in protective environments. (Photo: RoyBuri/Pixabay.)
evolution of foldable wings defines the group of Neoptera, which covers the Holometabola (fully metamorphosing insects) as well as the Polyneoptera (e.g. stick insects, roaches and termites) and the Paraneoptera (e.g. true bugs, lice and thrips). The fossil record features a major gap after the oldest known insect from 411 million years ago, so genetics and extrapolations from more recent finds are all that researchers can go by. Benjamin Wipfler from the Zoological Research Museum Alexander Koenig at Bonn, Germany, together with Sabrina Simon at Wageningen and others, has reported a large-scale phylogenomic analysis of Polyneoptera based on more than 3,000 protein-coding genes sampled from more than 100 insect species. The study aims to elucidate the evolution of 112 traits including diet, social behaviour, and habitat of larvae and adults, as well as the origins of flight (Proc. Natl. Acad. Sci. USA (2019) 116, 3024–3029). On the very origins of the first winglets that led to the evolution of flight, there have been several competing hypotheses, including one that involved gliding from trees to the ground, along with two others based on presumed aquatic stages, as can be observed in today’s dragonflies. Wipfler and colleagues conclude from
their findings that they can rule out an aquatic lifestyle for the common ancestor of winged insects. Thus, out of the three hypotheses, their results favour the glider one. This also fits with their finding that the common ancestor did not have anatomical adaptations typical of ground-living insects, such as a flattened underside, so are likely to have spent at least some of their life on plants. The data also suggest that some behaviours and lifestyles seen in several groups of insects, including social behaviours and life on plants, have evolved several times and are not ancestral. The same holds for the anatomical adaptation of ground-living insects. By contrast, the characteristic arrangement of biting mouthparts below the head capsule (orthognathy) is likely ancestral and has been more widely retained in Polyneoptera than in other groups. End of the insect world? In spite of this unrivalled success story lasting more than 400 million years, ecologists now have reason to worry about the declines observed in some orders such as the Lepidoptera (Curr. Biol. (2016) 26, R823–R825), and pollinating insects. Public perception and economic interests give prominence to bee problems,
Current Biology 29, R1105–R1121, November 4, 2019
R1107
Current Biology
Magazine Q&A
Xinnian Dong
Tobacco lover: The tobacco hornworm (Manduca sexta) has adapted to cope with the plant-produced insecticide nicotine, providing an example of a complex evolutionary relationship between plants and insects. (Photo: http://www.peakpx.com.)
even though the honey bee is just a domesticated species that humans can propagate as necessary. The observed losses in pollinators may, however, be just an indicator of wider extinction threats caused by the use of pesticides and the homogenisation of the environment. As Michael Engel has pointed out in the review cited at the beginning of this article, these rapid changes introduced by humans drive up extinctions and reduce the opportunities for speciation, undermining the long-running recipe for success of insects. Engel concluded: “Insects are better prepared to contend with an asteroid impact.” Because insects are so widespread and crucial in virtually every terrestrial ecosystem, their demise would have dramatic knock-on effects for life on Earth in general, not least for the survival of our own species. In this situation, on the verge of a possible man-made mass extinction, it is all the more important to understand how the diversity evolved and how it survived previous crises. “Studying insect ecology and evolution including co-evolution with plants has become even more important and urgent considering the increase in so-called ‘pest-species’ but also the dramatic decline of other insects caused by human impact,” Sabrina Simon concludes. “Only with a reliable phylogenetic reconstruction we can study how insect species influence ecosystems and sustain or endanger our natural resources.” In short, as we live on the planet of the insects, we’d better understand how it works. Michael Gross is a science writer based at Oxford. He can be contacted via his web page at www.michaelgross.co.uk
R1108
Xinnian Dong received her BS in Microbiology from Wuhan University in China in 1982 and her PhD in Molecular Biology from Northwestern University in Chicago, USA, in 1988. She began her study of plant immune mechanisms as a postdoc at the Massachusetts General Hospital at Harvard Medical School. Dong is currently an Arts and Sciences Professor of Biology at Duke University. She became an Investigator for the Howard Hughes Medical Institute (HHMI) and a Fellow of the American Association for the Advancement of Science (AAAS) in 2011, a member of the National Academy of Sciences (NAS) in 2012, and a Fellow of the American Academy of Microbiology (AAM) in 2013. What turned you on to biology in the first place? I grew up during the Cultural Revolution. It was such an ironic name for the period in China when any intellectual pursuit was suppressed. People with less knowledge controlled the lives of those with more. I remember my teenage years as aimless, with little studying in school. I could manage to get 100 points in an exam without ever opening the textbook. I was extremely lucky that the Revolution ended at the time when I was about to graduate from high school. I entered Wuhan University rather than being sent to the countryside or a factory. Due to this historical circumstance, I only became seriously interested in biology during my college years, especially after reading Molecular Genetics: An Introductory Narrative by Gunther Stent and Richard Calendar. The ingeniously simple experiments that were performed by these pioneers of molecular biology fascinated me so much that I wanted to become a molecular biologist myself. And what drew you to your specific field of research? I became very interested in immunology when I was in college, but I realized at the same time that I could not handle animal sacrifice. This was the reason that I decided to study plant immune mechanisms when Fred Ausubel offered me a postdoctoral position in his lab.
Current Biology 29, R1105–R1121, November 4, 2019
Who were your key early influences? My father had a significant early influence on me. He was an economist with a great vision for the future and deep scholarship. He was the one who encouraged me to study microbiology in college because he realized through his readings that molecular biology had become a major frontier in science and most of the early molecular studies were carried out in microorganisms. Both my father and my postdoctoral mentor Fred Ausubel trained many students and postdocs. I learned from them that one’s legacy can be extended through trainees. Do you have a scientific hero? I admire many scientists for their groundbreaking work, for example, Susumu Tonegawa’s discovery of somatic generation of antibody diversity. I hesitate to call these scientists my heroes because I do not have any information about them except for the work that made them famous. Do you have a favorite paper or science book? I already mentioned my favorite science book. Without searching too hard into my memory, my favorite paper is Witham et al.’s ‘The product of the tobacco mosaic virus resistance gene N: similarity to Toll and the interleukin-1 receptor’ (Cell (1994) 78, 1101–1115). In this paper, Barbara Baker’s laboratory reported the discovery of the first intracellular NB-LRR immune receptor in plants, and this is required for resistance to the tobacco mosaic virus (TMV) in tobacco plants. The genetic selection performed to identify the N gene was brilliantly designed and executed. More importantly, it suggested a possible role for Toll, which was known at the time to be only involved in controlling Drosophila development, in innate immunity. If you had not made it as a scientist, what would you have become? I admire the life of an artist and a writer because of the creative freedom associated with these two professions, but I have no special talent for either one. I am very happy being a scientist, especially a scientist supported by HHMI. I am pretty much free to explore things that are of interest to me.
Magazine Feature
Six-legged success stories Insects represent the majority of today’s animal biodiversity, although many of their species are now at risk from land-use change and pesticides. Given their vast number of species, it is no wonder that science is still busy finding new connections in their ecology and evolution, including in the ways they co-evolve with plants and other organisms. Michael Gross reports. Life on Earth, from our anthropocentric perspective, is often described as the evolution towards ‘higher’, more intelligent life forms including primates and then ourselves as the alleged pinnacle of creation. Alien visitors passing through the Solar System might first spot the green vegetation and measure its oxygen output. But anybody looking at species diversity, varieties of successful ecological strategies, and sheer number of individual animals would come to the conclusion that over the last 400 million years Earth has become the planet of the insects. There are more than a million described species in the class of insects (Ectognatha), which together with the less expansive Entognatha (around 5,000 species) comprise the Hexapods, or everything that has six legs. They outnumber all other species known to science, such that any project aiming to account for all eukaryotic species, like the Earth BioGenome Project (Curr. Biol. (2018) 28, R719– R721), will have to spend most of its time with insects. Research has uncovered a number of factors that have contributed to their spectacular success, as Michael Engel from the University of Kansas at Lawrence, USA, has explained in this journal (Curr. Biol. (2015) 25, R868– R872). Firstly, they suffered surprisingly few losses at higher phylogenetic levels during the last mass extinction — the one that defined the end of the Cretaceous and wiped out the non-avian dinosaurs among many other species. Thus, while much of the biodiversity we see around us, including birds and mammals, had only around 66 million years to diversify, insects go back more than 410 million years. In this timeframe, Engel reports, there have been several synergistic factors that enabled explosive growth of some groups at later points, without
triggering it directly. These include the first ever invention of flight, soon after the arthropod ancestors came out of the oceans, then, at a later point, complete metamorphosis, which led to the Holometabola groups now comprising more than 80% of insect diversity. Combined with an especially flexible development and the robust and versatile body plan based on the arthropod exoskeleton, these traits enabled insects to shape their world (Curr. Biol. (2017) 27, R283–R285) and interact with many other species in many different ways. Ants and plants In the Early Cretaceous (146–100 million years ago), flowering plants (angiosperms) spread around the world and pollinating insects have played an important part in this. Much of the current concern about population declines in insects is motivated by the
loss of pollinators that may ultimately threaten our food provision (Curr. Biol. (2018) 28, R1121–R1123). Over the same timescale, another kind of interaction evolved between many kinds of plants and many species of ants, where plants provide food and shelter, and ants offer defence and seed dispersal. They even protect plants from diseases (Oikos (2019) https://doi.org/10.1111/oik.06744). Research has shown that mutualism between ants (family of Formicidae, with more than 12,000 named species) and plants has enhanced diversification of plants, but its impact on the ants has been less clear-cut. Matthew Nelsen and colleagues at the Field Museum of Natural History at Chicago, USA, have addressed this question by analysing relevant traits in phylogenies covering more than 10,000 plant genera and 1,730 species of ants (Proc. Natl. Acad. Sci. USA (2018) 115, 12253–12258). Their results suggest a sequential series of events rather than a simultaneous boost for both sides. Ancestral ant species were carnivores nesting and foraging on the ground. Foraging on plants was the first relevant change, followed by accepting and looking for plant food. Omnivorous ants started to feed on plant sap and possibly on the honeydew produced by aphids (Curr. Biol. (2019) 29, R1–R3).
Plant like: Insects have adapted to many different forms and functions, including the striking camouflage of stick and leaf insects. The photo shows a giant prickly stick insect (Extatosoma tiaratum), a species endemic to Australia. (Photo: sandid/Pixabay.)
Current Biology 29, R1105–R1121, November 4, 2019
R1105
Current Biology
Magazine order that extend from Africa through to New Zealand. Appearances proved deceptive on the island of Madagascar as well. “The flamboyant stick insects of Madagascar, for instance, descended from a single ancestral species that colonised the island approximately 45 million years ago,” explains Sarah Banks from the group of Sven Bradler at the University of Göttingen. The oldest lineages of stick insects lead back to the time after the last mass extinction, 66 million years ago. This finding suggests that the characteristic camouflage evolved in response to the rapidly growing threat of birds and mammals taking over after the dinosaurs.
Green habitat: Acacias grow hollow spines (domatia), which ants use as shelter. (Photo: Ryan Somma/Flickr (CC BY-SA 2.0).)
Plant structures beneficial for ants only evolved later. These include extrafloral nectaries secreting nectar on stems or leaves: elaiosomes, which are food packages enticing ants to carry seeds with them, and domatia, hollow structures in which ants can nest, such as the spines formed by some species of acacias. These adaptations enabling ants to become fully engaged in a plant-based niche largely evolved in the Cenozoic, that is after the last mass extinction. Thus, the authors describe a stepwise increase in mutual dependence. During this tightening of the relations, the plants showed enhanced diversification rates, but the ants did not. In an effort to expand these studies to a wider range of species, Katrina Kaur and colleagues at the University of Toronto, Canada, have used text mining of more than 89,000 published abstracts to capture published traits associated with ant–plant mutualism (PLoS Comput. Biol. (2019) 15, e1007323). Like Nelsen and colleagues, their analysis suggests that ants diversified before becoming engaged in mutualistic relations with plants. “To our surprise, the intimate and often beneficial relationships that ants have with plants apparently did not help to generate the over 14,000 ant species on Earth today,” Kaur said. “Mutualism R1106
may put the brakes on the rise of new species or increase the threat of extinction because an ant’s fate becomes linked to its plant partner’s.” Leaves and sticks While ants developed many ways of living with and on plants, the group of leaf and stick insects (order Phasmatodea) evolved sophisticated ways of resembling plants in an effort not to be detected by predators hunting by vision. A relatively recent radiation has led to more than 3,000 species that may be very diverse visually, but are hard to sort into a phylogenetic tree based on existing sequence data. Therefore, the deeper connections of their evolutionary history have remained controversial. In a new study, Sabrina Simon from Wageningen University and Research, The Netherlands, and other researchers from around the world have analysed 27 new transcriptomes of Phasmatodea in combination with previously published sequence information (Front. Ecol. Evol. (2019) 7, 345). For each species, more than 2,000 separate genes were analysed. The results contradict some of the earlier divisions made on the basis of appearances. Instead, the new phylogenetic tree has a strong geographic division into western (New World) and eastern members of the
Current Biology 29, R1105–R1121, November 4, 2019
Termites and other cockroaches Insect orders have been shaken up and redefined in the last few decades as molecular studies forced revision of classifications based on anatomy and behaviour. As recently as 2007, molecular research confirmed that termites are just a eusocial group of cockroaches. While this relationship had been suspected since the early 20th century, it was not reflected in traditional systematics. Losing their status as a separate order, the termites were merged into the order Blattodea, which now includes around 4,400 species of cockroaches as well as more than 3,000 species of termites. Many of these species play important roles as degraders of dead wood, which also makes them noticeable players in the global carbon cycle and thus in climate regulation. Some termitederived enzymes are also of interest for the production of biofuel from otherwise indigestible biomaterials. Some Blattodea are also considered pests, and termites in particular can endanger wooden structures in some areas. Thus, there are many ecological and economical reasons to better understand their biology. Dominic Evangelista from the Sorbonne at Paris, France, and colleagues have recently presented a new, detailed phylogenetic analysis based on 2,370 protein-coding genes from 66 species representing all but one of the major groups of Blattodea (Proc. R. Soc. B (2019) 286, 20182076). “The analysis confirmed the new affiliation of termites within the cockroaches and clarified some
Current Biology
Magazine long-standing problems, including the relatively young age of the order,” says Sabrina Simon, who was a senior author of this study as well as the one on stick insects. While previous work had suggested origins some 240–180 million years ago, long before fossil evidence can be linked to it, the new study suggests that most major groups of Blattodea arose during the Cretaceous (147–66 million years ago), which is more easily reconciled with the fossil record. It also proves that any fossils resembling cockroaches in the Carboniferous (359–299 million years ago) can be safely excluded. Social behaviours like maternal brood care are not ancestral features of the group, the researchers find. Instead, they suggest that the common ancestor packaged its eggs in a protective parcel, the ootheca, and buried this in a hole, as many cockroaches still do today. This behaviour may also explain the evolution of wood-degrading behaviour, the authors say, concluding: “We suggest that the transition from a freeliving ancestor to living within wood (in Cryptocercus and termites) could have been partially driven by advantages gained in protection of the ootheca.” Zooming in on termites, and on the group of Termitidae in particular, Ales Bucek and Thomas Bourguignon from the Okinawa Institute of Science and Technology Graduate University, Japan, describe the origins of termite fungiculture elsewhere in this issue of Current Biology (https://doi.org/10.1016/j. cub.2019.08.076). The termite subfamily Macrotermitinae produces comb-like structures in its hives where they cultivate fungal symbionts. This, the authors find, is a derived feature probably unrelated to the earlier loss of protozoan symbionts in the termite gut. Origins of flight Some of the orders of insects have been a challenge to systematics, but the very root of the insects’ family tree poses even bigger and more fundamental questions. Key events here are the very first invention of flight in animals, which separated the Pterygota (winged insects) from the likes of silverfishes (order Zygentoma) and bristletails (order Archaeognatha). Early flying insects had stiff wings set at a fixed angle like today’s mayflies, damselflies and dragonflies. The
Social cockroaches: Termites are economically important for their ability to degrade wood. The evolution of this trait may be related to the habit of closely related cockroaches to bury their eggs in protective environments. (Photo: RoyBuri/Pixabay.)
evolution of foldable wings defines the group of Neoptera, which covers the Holometabola (fully metamorphosing insects) as well as the Polyneoptera (e.g. stick insects, roaches and termites) and the Paraneoptera (e.g. true bugs, lice and thrips). The fossil record features a major gap after the oldest known insect from 411 million years ago, so genetics and extrapolations from more recent finds are all that researchers can go by. Benjamin Wipfler from the Zoological Research Museum Alexander Koenig at Bonn, Germany, together with Sabrina Simon at Wageningen and others, has reported a large-scale phylogenomic analysis of Polyneoptera based on more than 3,000 protein-coding genes sampled from more than 100 insect species. The study aims to elucidate the evolution of 112 traits including diet, social behaviour, and habitat of larvae and adults, as well as the origins of flight (Proc. Natl. Acad. Sci. USA (2019) 116, 3024–3029). On the very origins of the first winglets that led to the evolution of flight, there have been several competing hypotheses, including one that involved gliding from trees to the ground, along with two others based on presumed aquatic stages, as can be observed in today’s dragonflies. Wipfler and colleagues conclude from
their findings that they can rule out an aquatic lifestyle for the common ancestor of winged insects. Thus, out of the three hypotheses, their results favour the glider one. This also fits with their finding that the common ancestor did not have anatomical adaptations typical of ground-living insects, such as a flattened underside, so are likely to have spent at least some of their life on plants. The data also suggest that some behaviours and lifestyles seen in several groups of insects, including social behaviours and life on plants, have evolved several times and are not ancestral. The same holds for the anatomical adaptation of ground-living insects. By contrast, the characteristic arrangement of biting mouthparts below the head capsule (orthognathy) is likely ancestral and has been more widely retained in Polyneoptera than in other groups. End of the insect world? In spite of this unrivalled success story lasting more than 400 million years, ecologists now have reason to worry about the declines observed in some orders such as the Lepidoptera (Curr. Biol. (2016) 26, R823–R825), and pollinating insects. Public perception and economic interests give prominence to bee problems,
Current Biology 29, R1105–R1121, November 4, 2019
R1107
Current Biology
Magazine Q&A
Xinnian Dong
Tobacco lover: The tobacco hornworm (Manduca sexta) has adapted to cope with the plant-produced insecticide nicotine, providing an example of a complex evolutionary relationship between plants and insects. (Photo: http://www.peakpx.com.)
even though the honey bee is just a domesticated species that humans can propagate as necessary. The observed losses in pollinators may, however, be just an indicator of wider extinction threats caused by the use of pesticides and the homogenisation of the environment. As Michael Engel has pointed out in the review cited at the beginning of this article, these rapid changes introduced by humans drive up extinctions and reduce the opportunities for speciation, undermining the long-running recipe for success of insects. Engel concluded: “Insects are better prepared to contend with an asteroid impact.” Because insects are so widespread and crucial in virtually every terrestrial ecosystem, their demise would have dramatic knock-on effects for life on Earth in general, not least for the survival of our own species. In this situation, on the verge of a possible man-made mass extinction, it is all the more important to understand how the diversity evolved and how it survived previous crises. “Studying insect ecology and evolution including co-evolution with plants has become even more important and urgent considering the increase in so-called ‘pest-species’ but also the dramatic decline of other insects caused by human impact,” Sabrina Simon concludes. “Only with a reliable phylogenetic reconstruction we can study how insect species influence ecosystems and sustain or endanger our natural resources.” In short, as we live on the planet of the insects, we’d better understand how it works. Michael Gross is a science writer based at Oxford. He can be contacted via his web page at www.michaelgross.co.uk
R1108
Xinnian Dong received her BS in Microbiology from Wuhan University in China in 1982 and her PhD in Molecular Biology from Northwestern University in Chicago, USA, in 1988. She began her study of plant immune mechanisms as a postdoc at the Massachusetts General Hospital at Harvard Medical School. Dong is currently an Arts and Sciences Professor of Biology at Duke University. She became an Investigator for the Howard Hughes Medical Institute (HHMI) and a Fellow of the American Association for the Advancement of Science (AAAS) in 2011, a member of the National Academy of Sciences (NAS) in 2012, and a Fellow of the American Academy of Microbiology (AAM) in 2013. What turned you on to biology in the first place? I grew up during the Cultural Revolution. It was such an ironic name for the period in China when any intellectual pursuit was suppressed. People with less knowledge controlled the lives of those with more. I remember my teenage years as aimless, with little studying in school. I could manage to get 100 points in an exam without ever opening the textbook. I was extremely lucky that the Revolution ended at the time when I was about to graduate from high school. I entered Wuhan University rather than being sent to the countryside or a factory. Due to this historical circumstance, I only became seriously interested in biology during my college years, especially after reading Molecular Genetics: An Introductory Narrative by Gunther Stent and Richard Calendar. The ingeniously simple experiments that were performed by these pioneers of molecular biology fascinated me so much that I wanted to become a molecular biologist myself. And what drew you to your specific field of research? I became very interested in immunology when I was in college, but I realized at the same time that I could not handle animal sacrifice. This was the reason that I decided to study plant immune mechanisms when Fred Ausubel offered me a postdoctoral position in his lab.
Current Biology 29, R1105–R1121, November 4, 2019
Who were your key early influences? My father had a significant early influence on me. He was an economist with a great vision for the future and deep scholarship. He was the one who encouraged me to study microbiology in college because he realized through his readings that molecular biology had become a major frontier in science and most of the early molecular studies were carried out in microorganisms. Both my father and my postdoctoral mentor Fred Ausubel trained many students and postdocs. I learned from them that one’s legacy can be extended through trainees. Do you have a scientific hero? I admire many scientists for their groundbreaking work, for example, Susumu Tonegawa’s discovery of somatic generation of antibody diversity. I hesitate to call these scientists my heroes because I do not have any information about them except for the work that made them famous. Do you have a favorite paper or science book? I already mentioned my favorite science book. Without searching too hard into my memory, my favorite paper is Witham et al.’s ‘The product of the tobacco mosaic virus resistance gene N: similarity to Toll and the interleukin-1 receptor’ (Cell (1994) 78, 1101–1115). In this paper, Barbara Baker’s laboratory reported the discovery of the first intracellular NB-LRR immune receptor in plants, and this is required for resistance to the tobacco mosaic virus (TMV) in tobacco plants. The genetic selection performed to identify the N gene was brilliantly designed and executed. More importantly, it suggested a possible role for Toll, which was known at the time to be only involved in controlling Drosophila development, in innate immunity. If you had not made it as a scientist, what would you have become? I admire the life of an artist and a writer because of the creative freedom associated with these two professions, but I have no special talent for either one. I am very happy being a scientist, especially a scientist supported by HHMI. I am pretty much free to explore things that are of interest to me.