© 2018. Published by The Company of Biologists Ltd | Journal of Experimental Biology (2018) 221, jeb170126. doi:10.1242/jeb.170126


Listening to Bach lights to all subsequent . In an that could teach us about brain extraordinary new paper in the journal function and through non- up brains Proceedings of the Royal Society B, invasive methods. may have Mehdi Behroozi from Ruhr University split from the mammalian evolutionary Bochum, Germany, and Brendon Billings tree nearly 300 million ago, but their from the University of the Witwatersrand, brains appear to be more in sync with South , recorded brain activity from those of , and possibly humans, than mildly sedated crocodiles while the previously thought. animals listened to tunes and watched a laser-light show, and the results hint that 10.1242/jeb.170126 these brain regions may have emerged Behroozi, M., Billings, B. K., Helluy, X., Manger, before birds and went their P. R., Güntürkün, O. and Ströckens, F. (2018). separate evolutionary ways. Functional MRI in the crocodile: a new avenue for evolutionary neurobiology. Proc. R. Soc. B 285, 20180178.

BRAIN EVOLUTION After ironing out a number of technical Daniel M. Vahaba (0000-0003-2960-3756) kinks, the international team of researchers University of Massachusetts Amherst In a ground-breaking first, researchers led by Felix Ströckens carefully placed [email protected] have measured brain activity in live juvenile Nile crocodiles into a brain crocodiles to understand how brains scanner in to measure brain activity. evolved to process sights and sounds. As Once the crocs were relaxed, the crocodiles are a recent ancestor of birds researchers presented a brief flash of red or Fly breath sets mites up and, more distantly, mammals, seeing green lights twinkling at different speeds for success how far back in evolutionary time brain while Behroozi and Billings watched how circuits originate in animals provides a their brain responded. Overall, the lights clue for when brains first started operating excited two suspected visual areas, as they do in . Although many including one ‘higher-order’ region that animals share brain molecules and cell responded more to red lights, suggesting types, the real test of brain conservation is subtle selectivity. These results are the first how similarly they function across to show visually triggered brain areas in species. For example, despite crocodiles; however, there was a lack of and brains being hugely different in clear evidence for hierarchal processing appearance, both are similarly wired, as observed in other animals or senses, resulting in them perceiving their such as hearing.

environment in analogous ways, namely SELECTION HOST in a hierarchical fashion. In order to expand the diversity of senses tested, the team then broadcasted several For parasites to thrive, they must first Hierarchical processing starts with simple sounds to the crocodiles in a separate part locate and then derive resources from a sensory information (e.g. tones, noises) of the study. The crocs listened to two host. Some parasites can use chemical being initially perceived in ‘earlier’ brain different simple sounds (random chord cues – such as CO2 released through regions, whereas complex sounds (e.g. noises at around 1000 or 3000 Hz), as respiration – to find hosts, and when music, language) solely activate well as one complex sound: a snippet multiple hosts live in the same area, downstream, ‘higher-order’ brain regions. from Johann Sebastian Bach’s parasites often preferentially infest certain Hierarchical processing is present in birds Brandenburg Concerto No. 4. Although individuals (or certain hosts are more and mammals, but until recently it was ‘lower’ auditory brain areas responded to resistant to parasite infestation). There are unclear at which point the brain pathways all three of the sounds, a ‘higher-order’ several characteristics that can make hosts were gained. Enter the crocodile, stage brain area responded solely to the more preferable for (or, alternatively, left. Crocodiles are the closest relatives to symphony in a similar region found in more vulnerable to) infestation by birds and haven’t shared a common birds and mammals that is similarly parasites, including specific behaviours, ancestor with mammals for nearly 300 selective for complex sounds such as poor overall health and being injured. million years. If crocodiles, birds and music and birdsong. However, whether parasites might be able mammals share similar brain regions to select hosts based on their metabolic important for processing sights and Taken together, these findings elevate rates – and, if so, whether they might sounds, it would suggest that these brain crocodiles’ status from fear-inducing, select hosts with high metabolic rates circuits were established early on in -blooded, modern-day to (which would produce resources for the evolutionary time and were passed down like-minded, informative and capable parasites at high rates) – remained

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1 OUTSIDE JEB Journal of Experimental Biology (2018) 221, jeb170126. doi:10.1242/jeb.170126 unknown. Because many parasites can mites can discriminate tiny differences in melanin for a boost in catecholamines? detect CO2 produced by hosts and odours produced by hosts and select the That’s what a group of researchers headed because CO2 production increases with victims that will produce the resources by William Jeffery from the University of metabolic rate, Collin Horn and two that they require most rapidly via higher Maryland, USA, wanted to find out. colleagues from the University of Alberta metabolic rates. If fruit flies think they’re in Canada wondered whether parasitic going to escape these bugs, they shouldn’t Jeffery and his colleagues had a hunch mites might be able choose specific fruit hold their breath – or maybe they should! that if cavefish brains had more of the fly hosts based on their relative CO2 catecholamine noradrenaline production. If so, they also wondered 10.1242/jeb.170100 (norepinephrine), it might help the whether higher metabolic rates in injured Horn, C. J., Mierzejewski, M. K. and Luong, L. T. stay alert longer to seek out food and flies might underlie the mites’ (2018). Host respiration rate and injury-derived mates, both of which are in scarce supply documented preference for hurt hosts. cues drive host preference by an ectoparasite of deep underground. Noradrenaline is a fruit flies. Physiol. Biochem. Zool. 91, 896-903. stimulating neurotransmitter best known To answer their first question, the Molly H. B. Amador (0000-0003-0621-3528) for heightening an ’s senses during researchers first determined the resting University of Miami stress. Jeffery already knew that it takes a metabolic rate of individual flies by [email protected] lot longer for an albino laboratory mouse measuring each one’sCO2 production in a to succumb to anaesthesia than a regular tiny respirometer. Then, they placed a mouse, and he faced similar challenges parasitic mite at the base of a Y-connector Cavefish compromise with his albino cavefish compared with and immobilized two fruit flies with the fully pigmented surface fish. So, the different metabolic rates at the other end colour for catecholamine- researchers used the length of time it takes of the connector – one fly in each arm – kick a fish to reach unconsciousness under creating a two-choice tunnel for the mite. anaesthetic as a proxy for alertness and set After an hour, the group inspected the flies about testing the trade-off hypothesis. under a microscope to see which fly the mite had chosen. Horn and his colleagues The team began by measuring found that the mites did indeed tend to noradrenaline in A. mexicanus brains and infest the fly with the higher metabolic rate, confirmed that albino cavefish brains do suggesting that these parasites can detect have more of this catecholamine than the not only the presence of CO2,butalso brains of surface fish, as predicted by the small differences in CO2 concentration. trade-off hypothesis. When the team gave albino cavefish a drug to block To determine whether mites might be noradrenaline receptors, they found that ’ attracted to injured flies because of TRADE-OFF the cavefish s tolerance for anaesthesia increases in the flies’ metabolic rates decreased, meaning the cavefish struggled during healing, Horn and his colleagues We’re all the same colour with the lights to stay alert without noradrenaline measured the metabolic rates of flies that off. This sentiment is literal for many signalling in the brain. In contrast, when the had been punctured with a pin. animals that live in constant darkness team supplemented the pigmented surface Unexpectedly, they found that metabolic because the loss of the skin pigment, fish with an extra dose of noradrenaline, rate did not change in injured flies, melanin, is commonplace. For example, these fish resisted the anaesthetic longer, indicating that mites must use another cue certain populations of the Mexican tetra becoming more like their albino relatives. to detect injured hosts. fish, Astyanax mexicanus, live in isolated underground caves that never see the light Jeffery’s team now needed to link To further determine what might attract of day and have evolved to have little to no decreased melanin production with their mites to wounded flies, the scientists placed pigment in a very short time. But other observations of heightened alertness in either haemolymph (equivalent to fruit fly populations of A. mexicanus living in noradrenaline-loaded brains. is blood) or water on the bodies of uninjured sun-lit surface pools still produce normal caused by a mutation in a gene called flies. They then allowed mites to choose amounts of melanin. In fact, albinism is an oca2, which encodes a protein that between haemolymph- and water-treated extremely rare condition because it leads to regulates L-tyrosine delivery to melanin- flies in the same Y-connector setup used in a host of health complications beyond a producing cells. So, the scientists used a the first experiment. The researchers found sunburn. There must be some advantage, molecular tool to knockout the oca2 gene that the mites preferentially infested flies then, to shutting off melanin synthesis in a in surface fish, making them albino. that had received a drop of haemolymph, lightless world. One intriguing explanation When the researchers presented these suggesting that these parasites rely on is the melanin–catecholamine trade-off mutated surface fish with anaesthetic, chemical cues from the injury itself to find hypothesis. Catecholamines are they found that it took these fish a long vulnerable hosts. neurotransmitters that play a key role in time to reach unconsciousness, just like in brain function. Because both of these the naturally albino cavefish. Overall, Horn and the other researchers molecules are synthesized from the same discovered that this common parasite of amino acid, L-tyrosine, less melanin So Jeffery’s group has confirmed that fruit flies is able to use both exhaled and production leaves more L-tyrosine decreasing melanin synthesis in cavefish ‘leaked’ chemicals to pick the perfect available for catecholamine synthesis. But enables the fish’s brain to make more host. Their results also suggested that the why are cavefish willing to sacrifice noradrenaline from L-tyrosine, and this Journal of Experimental Biology

2 OUTSIDE JEB Journal of Experimental Biology (2018) 221, jeb170126. doi:10.1242/jeb.170126 additional noradrenaline helps them fight everything about navigation. A recent termed a ‘micro’ call, was shorter and had off drowsiness, a great advantage for cave study suggests that ‘whisper’ or even a much lower sound pressure level life. Unfortunately, we surface dwellers completely switch off echolocation under (volume) than known echolocation calls. will have to settle for a double espresso to certain circumstances and fly ‘blind’, Importantly, the low pressure level eke out a few more hours from the day! which could explain the high percentage drastically reduces the detection range, of bats killed by wind turbines. making the call ineffective for flight 10.1242/jeb.170092 navigation at high speed or insect Bilandžija, H., Abraham, L., Ma, L., Renner, K. J. Aaron Corcoran from the Wake Forest detection. And, in the cases in which the and Jeffery, W. R. (2018). Behavioural changes University, USA, and Theodore Weller bats flew into the mist-net that the controlled by catecholaminergic systems explain researchers deployed as an obstacle, they recurrent loss of pigmentation in cavefish. Proc. from the USDA Forest Service Biol. Sci. B 285, 20180243. investigated the use of echolocation in were either using the micro calls or no hoary bats, the species that is killed most calls at all when approaching the net and Sarah Alderman (0000-0002-8896-9777) frequently by wind turbines in the USA. echolocation was only used shortly before University of Guelph – [email protected] The researchers performed a series of the collision occurred too late to avoid three experiments recording bat calls and being caught. their flight paths: (1) under natural Whisper in the dark conditions, (2) in response to an As the study took place during the hoary introduced obstacle and (3) in response to bat mating season and the researchers echolocation playbacks. Previous field recorded the micro calls when the recordings had suggested that bats might bats were approaching members of their not always use echolocation, but these own species or when flying towards a observations had been challenged speaker that was playing bat calls, the because it was not clear whether the bats researchers concluded that bats might were always in the range of the produce micro calls to avoid other bats microphones. Therefore, the researchers eavesdropping on their conversations of the current study used a combination of during the mating season. Although micro calls would still allow bats to time-synchronised ultrasound detect trees from a distance of 7.5 m, microphones and infrared cameras. The which is early enough to avoid a cameras captured the exact flight path of ECHOLOCATION collision, the situation might be the bats and, together with the known different, unfortunately, when it comes position and the recording direction of the In 1938, a young from Harvard to rotor blades moving at high speed, microphones, they were able to determine University solved a mystery that was first and might partly explain the high the exact location that each recorded call described in the 18th century, when number of hoary bats killed by wind zoologists discovered that bats with was made from. turbines in the autumn breeding season. experimentally blocked ears crash into objects, whereas blinded bats can Surprisingly, Corcoran and Weller only 10.1242/jeb.170076 navigate just fine. The student, Donald recorded examples of previously known Griffin, found out what is general hoary bat echolocation calls in 8% of the recorded flights and the bats flew about Corcoran,A.J.andWeller,T.J.(2018). knowledge today: bats echolocate to Inconspicuous echolocation in hoary bats navigate, i.e. they send out sound waves half of the time without any recordable (Lasiurus cinereus). Proc. Biol. Sci. 285, and use the echo that is produced when echolocation. Furthermore, the scientists 20180441. the sound waves hit an object to find detected a previously unknown call type Julia Nowack (0000-0002-4512-5160) obstacles in their flight path. But it that the bats used in the remaining 43% of University of Veterinary Medicine Vienna appears that we still do not know recorded flights. The call, which they [email protected] Journal of Experimental Biology