Mantises See in 3D, but Not Like You and Me

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Mitochondria are too hot Because of the controversial nature of their Sick ants save findings, Crétien and his colleagues to handle! decided to use various chemicals to impair themselves by acid- mitochondrial function, while monitoring spraying their sisters heat generation using the same fluorescent dye, in order to ensure that their results were real and not due to a faulty organelle or artifacts caused by the dye. To eliminate the possibility that the changes in MTY fluorescence were due to changes in pH and membrane potential of the mitochondria during respiration, the authors treated the human kidney cells with cyanide, oligomycin or respiratory enzyme inhibitors such as rotenone and antimycin MITOCHONDRIA – which are known to affect the

mitochondria by altering membrane SICKNESS BEHAVIOUR Back in 1957, in his article published in potential, changing the mitochondrial pH, Scientific American (volume 197, disrupting membrane structure and Nurseries are notorious hotbeds of disease pp. 131–144), biologist Philip Siekevitz affecting the function of the mitochondrial and contagion. Place one snotty child in a called the mitochondrion the ‘powerhouse respiratory enzymes. Indeed, the authors room with 10 healthy kids and you’re on of the cell’, a term very much used today found that MTY fluorescence correlated the cusp of an epidemic. Now imagine this when we talk about this complex with mitochondrial respiration and that it nursery multiplied by hundreds and you’ll organelle. Mitochondria are organelles that was not due to faulty mitochondria or have an idea of life inside an ant colony, use oxygen and nutrients to generate artifacts in the fluorescence. The where sick ants can easily transmit energy and heat to maintain a stable body researchers further validated their findings pathogens to their sisters. To reduce this temperature. But did you ever wonder how when the response of the dye was enhanced risk, ants use different strategies to detect hot they actually get when they ‘work’ to in the presence of proteins involved in heat and disinfect diseased nestmates, heat us up? A group of researchers did, and generation. Therefore, MTY seems to effectively acting as nurses, executioners their findings are extraordinary: work, and work well, when it comes to or morticians. But what if the nurse mitochondria can heat up to close to 50°C, monitoring mitochondrial heat generation herself is infected? Will she fall victim to even though our core temperature is closely and mitochondria really do seem to run hot disease or can she act to reduce her risks of maintained at 37.5°C. when they are generating energy. further decline? The answer, as shown in an exciting new paper in PNAS by Dominique Crétien, a researcher working Through their work, Crétien and his Matthias Konrad and his colleagues from with Pierre Rustin at the Université Paris 7 the Institute of Science and Technology in in France, along with a team of colleagues have raised even more questions about heat regulation in vertebrates. How Austria, is that it depends on what her international researchers, decided to patient is infected with. investigate how hot mitochondria actually can the mitochondrial enzymes perform so get when they generate heat in healthy efficiently at such high temperatures? What human cells. To do so, the authors used a implications do these findings have for Konrad and his colleagues began by brand-new dye that targets the mitochondrial structure and function? How exposing ants to one of two different mitochondria and changes its do they affect (if at all) how we approach fungal pathogens. The first, called fluorescence with temperature, called mitochondrial disorders and how we treat Metarhizium, kills ants rapidly, while the them? One thing is certain, though: the Beauveria MTY. When the researchers monitored ‘ ’ second, called , causes only the fluorescence of the dye during cellular term powerhouse just got a whole new minimal mortality. When ants infected respiration in a human kidney cell line, meaning. with one pathogen were subsequently they found that mitochondria are able to 10.1242/jeb.170027 co-infected with the other, known as a function at temperatures that are heterologous infection, things got much approximately 10°C higher than the core Crétien, D., Bénit, P., Ha, H.-H., Keipert, S., worse and mortality rates shot up. This, in El-Khoury, R., Chang, Y.-T., Jastroch, M., Jacob, body temperature. The group recorded H. T., Rustin, P. and Rak, M. (2018). Mitochondria itself, is not surprising. Co-infection often this result multiple times and determined are physiologically maintained at close to 50°C. elevates mortality because it forces that, as long as the mitochondria are PLOS Biology 16, e2003992. animals to simultaneously solve distinct functional and have optimal conditions, Oana Birceanu immunological problems. But what was they indeed increase their temperature Wilfrid Laurier University surprising is that the singly infected ants during normal functioning. [email protected] behaved as if they were aware of the added

Outside JEB reports on the most exciting developments in experimental biology. The articles are written by a team of active research scientists highlighting the papers that JEB readers can’t afford to miss. Journal of Experimental Biology

1 OUTSIDE JEB Journal of Experimental Biology (2018) 221, jeb170027. doi:10.1242/jeb.170027 dangers of a heterologous infection – and Birds and mammals expressed genes in the mesopallium – a acted to reduce it. region of the brain involved in higher- share smartly designed order processing. Briscoe found a To examine the possibility that singly neurons whopping 78 genes that were uniquely infected ants are risk adverse, the team and highly expressed in the mesopallium. confronted them with a nestmate carrying The team then focused on five of the more the other pathogen. What they found was highly expressed unique genes and both amusing and sensible. In short, singly mapped out their expression visually to infected ants are cranky, just like any other gain a bird’s eye view of how well it sick animal. In contrast to their relatively distinguished the mesopallium from docile uninfected counterparts, singly surrounding brain areas. The stained infected ants bite, grab and drag their brains revealed that the top five genes nestmates about. Worse still, they spray their cleanly delineated the mesopallium from infected nestmates with an antimicrobial other surrounding brain regions, poison, especially if their nestmates carry suggesting the genes are important heterologous infections. Both types of genetic markers for the special cell types response are sophisticated and effective. NEURON ARCHITECTURE that comprise mesopallium.

Konrad and his team argue that becoming Birds can do most things just as well as One caveat is that chickens are lower in ornery is part of a suite of adaptive mammals. Crows use tools to solve the cognitive pecking order compared to responses called ‘sickness behaviors’ that complex puzzles. Lyrebirds are expert the linguistic abilities of vocal learning involve things like crankiness, lethargy vocal mimics, putting polyglots to shame. avians, such as songbirds. As a follow-up, and a diminished appetite. By reducing And even the humble pigeon is a the team confirmed that expression of the activity and keeping others at bay, discerning enough art critique to same genes delineated mesopallium in the ‘sickness behaviors’ are thought to help distinguish between paintings by Picasso European starling, a songbird with an animals fight infection. At the same time, and Monet. Nevertheless, birds still get a extensive vocal repertoire, suggesting acid spraying serves two crucial functions. bad rap. Calling someone a ‘bird brain’ these genes are conserved across birds. First, ants that spray have fewer fungal insults their intelligence due in part to bird spores transmitted to them. This lowers brains not having the fanciful folds and While the avian mesopallium and their risk of heterologous co-infection more layers found in mammal brains. mammalian cortex originate from the than twofold, thereby forestalling a same brain region early in life premature death. Second, because sprayed The neocortex, the outer layer of (telencephalon), they take on different ants are disinfected, they become less mammalian brains, is often touted as shapes across development: the cortex dangerous to the rest of the colony. being the hallmark of a mammal’s becomes layered in mammals, whereas advanced cognition. It’s the largest part of clusters of neurons assemble in birds People have a natural aversion to sickness. human brains, and is thought to give rise (referred to as ‘nuclei’). Therefore, Watch the horror in passengers’ eyes when to primates’ advanced intellectual Briscoe and colleagues examined whether someone sneezes on the subway without abilities. As bird brains are smooth and mouse cortex expressed a similar genetic covering their nose and mouth! But we are without layers, it was long presumed signature to that which characterized the generally don’t distinguish between they were behind the times and that their mesopallium. Lo and behold, expression specifictypes of contagion, simply because neurons didn’t play a similar function or of the same five genes that distinguished we don’t know which of the myriad of come from a similar evolutionary origin to the mesopallium outlined the mouse diseases our fellow travelers are carrying. mammals. cortex as well, suggesting the neurons are Did the sneeze indicate flu, the common cut from the same evolutionary cloth. cold or something as benign as a snuffle of However, scientists have begun to peck dust? We can’t tell. But remarkably, away at this ancient notion of ‘bird brain’ The research is fascinating as it suggests infected ants can tell, and moreover they being an insult. In a recent paper that birds and possibly primates evolved then use this recognition to dictate their published in Current Biology, Steven intelligence independently and that behavior. At present, the authors don’t Briscoe, working in the lab of Clifton cortical neurons may be as ancient as the understand the mechanisms that regulate Ragsdale at the University of Chicago, last common ancestor shared by birds and this complex feedback, but finding out USA, demonstrated that birds, mammals mammals. In short, neurons just took on promises to be an exciting journey. and reptiles all share similar brain cells in different architecture for bird brains, but it the cognitive cortex, challenging old doesn’t make them any less brilliant. 10.1242/jeb.169946 ideas about avian aptitude, anatomy and ancestry, and suggesting that ‘bird brain’ 10.1242/jeb.170001 Konrad, M., Pull, C. D., Metzler, S., Seif, K., should really be a compliment. Briscoe, S. D., Albertin, C. B., Rowell, J. J. and Naderlinger, E., Grasse, A. V. and Cremer, S. Ragsdale, C. W. (2018). Neocortical association (2018). Ants avoid superinfections by performing cell types in the forebrain of birds and alligators. risk-adjusted sanitary care. Proc. Natl. Acad. Sci. To start, Briscoe and his team first Curr. Biol. 28, 686-696.e6. USA 115, 2782-2787. evaluated whether any genes were Daniel E. Rozen specially enriched in the brain of an Daniel M. Vahaba Leiden University evolutionarily ancient bird: the chicken. University of Massachusetts Amherst

[email protected] Specifically, they focused on uniquely [email protected] Journal of Experimental Biology

2 OUTSIDE JEB Journal of Experimental Biology (2018) 221, jeb170027. doi:10.1242/jeb.170027

Mantises see in 3D, but experience 3D movies. In Nityananda’s Highways and byways experiments, both humans and mantises not like you and me saw complex dot patterns where a into thin air for songbirds camouflaged and moving target spiralled into view. The patterns could be adjusted so the target appeared far away or close up, and the human participants would say whether it was close or far, while the mantises expressed their response by trying to catch the tasty, but fake, ‘prey’ target when it came within their striking range (∼2.5 cm).

The researchers showed that both humans VISION

and mantises could see the 3D targets when OXYGEN TRANSPORT the dot patterns that were seen by the two Praying mantises are inarguably one of eyes were similar. However, when The harsh environment and thin air of the coolest insects: lurking about, still as Nityananda inverted the brightness in one mountain landscapes and highland statues, waiting to snatch their oblivious eye, making it look like a photo negative, the plateaus is a fertile testing ground for prey unawares. Researchers at Newcastle humans were completely derailed. Their broad evolutionary questions about how University, UK, have managed to dial-up trusty luminance cues were wrong and they animals scrape by in hostile the mantis coolness factor one notch couldn’t judge depth. But, the mantises kept environments. Evolution comes with a lot further. They outfitted these tiny assassins attacking their prey. Clearly, they were of baggage and different species may hit with miniscule 3D glasses to uncover that exploiting another cue. Next, the researchers upon unique solutions to common mantises use a completely novel form of showed both groups two completely problems simply because they had 3D vision when capturing their prey. different dot images. For humans, this was different ancestral starting points. For very confusing, as the brain couldn’tmake small, active songbirds, a perennial Many visual cues can be exploited to help comparisons between different images in problem at high altitude is supplying judge how close or far an object is in the each eye. Human performance was enough oxygen to fuel metabolism. world. One way that depth is processed is abysmal, but the mantises remained unfazed through stereopsis: each eye sees a slightly by the researchers’ attempts to thwart their Haemoglobin is critical to oxygen different view of the world and the brain vision. The team concluded that mantises transport. It is responsible for shuttling can identify these differences. Human might not compare the details of the entire oxygen collected in the lungs to the rest of stereoscopic vision specifically uses imageineacheye;whatseemedtomatter, the body and is implicated in adaptation to differences in luminance or brightness to instead, was motion. Mantises were picking low oxygen (hypoxia). Many animals that help judge depth in the world. Stereopsis up on changes in light patterns linked to are well adapted to hypoxia have isn’t an easy task and it is computationally object motion and not the picture details haemoglobins with high oxygen binding expensive, which might help explain why behind the motion –something that humans affinities. An international team of numerous vertebrates like humans and are simply unable to do. researchers led by Jay Storz from the macaques use stereopsis, but mantises are University of Nebraska, and Fumin Lei, the only insects known to use it. This It is important to accurately judge depth from the Chinese Academy of Sciences unique ability captured the attention of when you are an ambush predator like a and the University of Chinese Academy Vivek Nityananda and his colleagues at praying mantis. Fumbling your prey of Sciences, compared haemoglobin Newcastle University’s Institute of might mean you go hungry or alert other, function in high- and low-altitude birds to Neuroscience, who were amazed that bigger, predators waiting nearby. Mantis find out whether changes in haemoglobin mantises, with only about a million hunting style, ‘sit-and-wait’, might have function had similar molecular bases in neurons (compared with our ∼100 billion), selected for this novel, motion-based form different evolutionary lineages. could do such computations. of stereoscopic vision. Great for mantises, this new 3D vision is less computationally The team collected muscle and blood The researchers set out to test whether costly. The research team thinks the samples from 17 species of tit from high- mantis stereovision was similar to that of simpler form of vision will have exciting altitude sites on the Qinghai-Tibet humans, or whether they had evolved a applications for streamlining the visual plateau, in the mountains of southwestern new solution to seeing in 3D. Using some depth algorithms used in robotics. China, and from lowlands throughout of the smallest 3D glasses imaginable, the eastern China. They extracted researchers presented mantises with 10.1242/jeb.170019 haemoglobin from the blood samples and special stereopsis movies (which control Nityananda, V., Tarawneh, G., Henriksen, S., subjected it to a battery of tests to for and eliminate other depth cues) in a Umeton, D., Simmons, A. and Read, J. A. C. characterize its oxygen binding custom-made insect cinema. The 3D (2018). A novel form of stereo vision in the praying properties. As haemoglobin function is glasses allowed the researchers to show a mantis. Curr. Biol. 28, 588-593. sensitive to subtle differences in the chain slightly different image to each eye, Erin McCallum of amino acids that comprise the protein, creating the illusion of a 3D object in their Umeå University the team also sequenced the haemoglobin visual field – exactlythewaywe [email protected] genes for each species from portions of Journal of Experimental Biology

3 OUTSIDE JEB Journal of Experimental Biology (2018) 221, jeb170027. doi:10.1242/jeb.170027 muscle. Next, they constructed a increased. However, the team identified enough to make a fully fledged, modern haemoglobin family tree to suss out the one case where a pair of species found highland haemoglobin: additional evolutionary relationships between the the same solution for living the high life. substitutions were essential for high- haemoglobins. Finally, the team Both the grey-crested tit, Lophophanes altitude adaptation. manufactured their own haemoglobin dichrous, and the ground tit, Parus with custom sequence mutations to match humilis, swapped a threonine residue for High-altitude birds take quite a few specific changes in the amino acid an alanine residue at position 34 in one liberties with the biochemical properties sequence with effects on oxygen binding of the two chains of amino acids that of their haemoglobin, considering it’sso affinity. comprise haemoglobin, but this integral to oxygen transport and survival. substitution was absent in their lowland Even in the rare cases where elements are The haemoglobin of the species that live cousins. Intrigued, the researchers shared, different families still rely on at high altitude had a higher affinity for tested whether this modification had any subtle twists to get it just right. In solving oxygen than that of their lowland consequences for oxygen transport by the riddle of life in thin air, birds of a relatives, meaning that their blood was reconstructing the haemoglobin of the last feather do not flock together. better at grabbing onto oxygen, a useful common ancestor shared by the grey- feature for life in hypoxia. The high- crested tit and ground tit and comparing its 10.1242/jeb.170324 altitude haemoglobins also displayed a functional properties with those of the tits’ Zhu, X., Guan, Y., Signore, A. V., Natarajan, C., slew of amino acid substitutions absent haemoglobins. Both of the living species DuBay, S. G., Cheng, Y., Han, N., Song, G., Qu, Y., from those of the low-altitude species. had haemoglobin with higher affinity for Moriyama, H., et al. (2018). Divergent and parallel routes of biochemical adaptation in high- Different branches of the family tree oxygen than that of their ancestor, but the altitude passerine birds from the Qinghai-Tibet generally had unique sets of differences were attributable to other Plateau. Proc. Natl. Acad. Sci. USA 115, substitutions, suggesting that there are amino acid alterations elsewhere in the 1865-1870. multiple, independent molecular amino acid chains. While the substitution Brittney G. Borowiec pathways by which the affinity of at position 34 alone improved the affinity McMaster University haemoglobin for oxygen can be of haemoglobin for oxygen, it wasn’t [email protected] Journal of Experimental Biology