Going a bit batty – How do bats withstand so many viruses?

Dr Michelle Baker from the CSIRO Australian Animal Health Laboratory spoke at Macquarie University last week about her work on bat immune systems. Her lab recently contributed to the high impact Hendra virus vaccine for horses. Dr Baker’s work has implications for disease control and prevention and management of virus spillovers into human communities worldwide.

Bats make up 20% of mammalian diversity, are long lived for their body size and are the only mammals with powered flight. Bats are vital to ecosystem functions such as pollination, fertilisation and insect control (Calisher et al. 2006). Despite these unique characteristics they are not intensively studied like most other mammal groups. Before Dr Baker’s research group focused on bats not much was known about their immune systems (Baker et al. 2013).

Figure 1. Possible virus transmission routes from bats to humans. (adapted from image presented by Dr Michelle Baker)

Figure 1. Possible virus transmission routes
(adapted from image presented by Dr Michelle Baker).

Bats act as viral reservoirs, meaning they carry a range of viruses (He et al. 2010; Ng & Baker 2013). Fatal human viruses that can be traced back to bats include Rabies, Hendra, Ebola, Marburg and the SARS coronavirus (Ng & Baker 2013). These viruses occasionally spill over from bats into other animals and that’s normally how humans become infected (Figure 1). But even with this load of up to 100 different viruses, bats are hardly ever sick (Baker et al. 2013).

The bat’s lack of symptoms from viral infections was puzzling, so Dr Baker’s team looked more closely at bat immune systems. When a viral infection occurs in other mammals the immune system quickly delivers a generic response (innate response) and then a specific response occurs more slowly (adaptive response; Katze et al. 2002). The researchers observed that bats don’t develop many antibodies in response to infections, so they thought the bat immune system might be knocking down the viruses before the immune system could mount an adaptive response (Baker et al. 2013).

Figure 2. The Black Flying Fox, Pteropus alecto.

Figure 2. The Black Flying Fox, Pteropus alecto.

To test this idea the researchers sequenced the genomes and studied the immune responses of two species of bat: Myotis davidii, a micro bat, and Pteropus alecto, a megabat (Figure 2). They found the collection of immune genes in bats is different to other mammals. For example, bats have fewer genes for interferon production (Papenfuss et al. 2012).

Interferon is a protein produced by the immune system in response to the detection of viral invaders. It starts a signaling cascade that creates an anti-viral state in cells (He et al. 2010; Figure 3). High interferon levels can be toxic for cells, so normally the interferon level is very low. When a viral infection is detected, the interferon level is dramatically increased which signals cells to start fighting the infection (Katze et al. 2002). There are multiple types of interferon, but the type Dr Baker spoke most about is interferon alpha (IFNA).

Figure 3. Interferon signaling cascade - causes expression of immune system genes and creates an antiviral state in cells (Katze et al. 2002).

Figure 3. Interferon signaling cascade – causes expression of immune system genes and creates an antiviral state in cells (Katze et al. 2002).

In contrast to expectations, bat cells were found to have their IFNA genes constantly switched on and there is no increase when cells are infected with viruses (Figure 4). Even with this high IFNA level the toxicity effect observed in other mammals isn’t seen in bats. This IFNA level in bats may be part of the reason they can carry so many viruses, but don’t often get sick from them. Other research groups have found that bat IFNA genes have been positively selected which means they must have been beneficial to bats as they lived with viruses in the past (Calisher et al. 2006; He et al. 2010). Recent work has hypothesised that there is a link between the evolution of flight and the ability of bats to harbor viruses without becoming sick (Zhang et al. 2013; O’Shea et al. 2014).

These findings were very new and unexpected so there were lots of questions from the audience after the seminar. It seems like everywhere Dr Baker turned there were more questions! These are the ‘top 5’ questions asked:

  1. Why aren’t the bats harmed by high levels of interferon in uninfected cells like other mammals?
  2. What triggers the spillover of viruses into other animals that cause outbreaks?
  3. Could there be a link between the interferon level and their long lifespan relative to their body size?
  4. What is the bat immune response to bacterial infection?
  5. Why doesn’t the bat immune response completely wipe out the viruses? How come the viruses can persist and then spill over into other animals?
Figure 4. Interferon alpha levels in infected and uninfected cells in bats and other mammals  (adapted from image presented by Dr Michelle Baker).

Figure 4. Interferon alpha levels in infected and
uninfected cells in bats and other mammals
(adapted from image by Dr Michelle Baker).

So much is currently unknown about how bats can carry so many viruses without being sick. Dr Baker and her team are working to find answers to these questions and more. As human populations increasingly overlap with bat habitats there is more chance of spillover events affecting human and animal populations. Dr Baker’s research could be used to understand human responses to viruses and develop anti-viral treatments in the future.

Learn more:

Baker ML, Schountz T & Wang L-F (2013). Antiviral Immune Responses of Bats: A Review. Zoonoses and Public Health, 60, 104-116. doi: 10.1111/j.1863-2378.2012.01528.x

Calisher CH, Childs JE, Field HE, Holmes KV & Schountz T (2006). Bats: Important Reservoir Hosts of Emerging Viruses. Clinical Microbiology Reviews, 19(3), 531-545. doi:  10.1128/CMR.00017-06

He G, He B, Racey PA & Cui J (2010). Positive Selection of the Bat Interferon Alpha Gene Family. Biochemical Genetics, 48(9-10), 840-846. doi: 10.1007/s10528-010-9365-9

Katze M, He Y & Gale M (2002). Viruses and interferon: A fight for supremacy. Nature Reviews Immunology, 2(9), 675-687. doi: 10.1038/nri888

Ng J & Baker ML (2013). Bats and bat-borne diseases: a perspective on Australian megabats. Australian Journal of Zoology, 61, 48-57. doi: 10.1071/ZO12126

O’Shea T, Cryan P, Cunningham A, Fooks A, Hayman D, Luis A, Peel A, Plowright R, & Wood J (2014). Bat Flight and Zoonotic Viruses. Emerging Infectious Diseases, 20(5), 741-745. doi: 10.3201/eid2005.130539

Papenfuss AT, Baker ML, Feng Z-P, Tachedjian M, Crameri G, Cowled C, Ng J, Janardhana V, Field HE, Wang L-F (2012). The immune gene repertoire of an important viral reservoir, the Australian black flying fox. BMC Genomics, 13:261, doi: 10.1186/1471-2164-13-261.

Zhang G, Cowled C, Shi Z, Huang Z, Bishop-Lilly KA, Fang X, Wynne JW, Xiong Z, Baker ML, Zhao W, Tachedjian M, Zhu Y, Zhou P, Jiang X, Ng J, Yang L, Wu L, Xiao J, Feng Y, Chen Y, Sun X, Zhang Y, Marsh GA, Crameri G, Broder CC, Frey KG, Wang L-F & Wang J (2013). Comparative Analysis of Bat Genomes Provides Insight into the Evolution of Flight and Immunity. Science, 339, 456-460. doi: 10.1126/science.1230835

Silhouette images in Figure 1 sourced from: horse, bat, pig, humans.

Playing well with others? Sociality in huntsman spiders

Why do some huntsman spiders live in groups while the majority are perfectly happy living a solitary life? Dr Linda Rayor from Cornell University in New York spoke at Macquarie University recently about her work with Australian social huntsman spiders (Delena cancerides) and her excitement about finding more social huntsman species in Australia last year. Dr Rayor is passionate about social spiders and her findings could shed light on the evolution of parental care in a broad range of animals.

Sociality in arachnids is very rare – less than 1% are social beyond a short time of maternal care just after hatching. This may be due to the challenges a spider species has to overcome to become social. Aggressiveness in spiders means the majority can’t tolerate any other spiders being around them and this can lead to cannibalism (Riechert & Lockley 1984). The existence of three social huntsman species in Australia is a ‘big deal’ according to Dr Rayor as they have overcome the inbuilt aggressiveness that seems to come naturally to so many spiders.

Sociality in spiders has evolved independently at least 18 times (Yip & Rayor 2013b), so there must be something in it. Social huntsman spiders are found in south-west and south-eastern Australia and live in groups of 20 to 200 individuals, with a dominant female and her offspring of all different ages. In contrast to social insects, such as bees and termites, living together doesn’t increase the reproductive output of social spiders so there must be a different driving force behind their sociality (Whitehouse & Lubin 2005).

Delena Cancerides collected at Mount Ainslie, ACT in March 2014 Source: Canberra Times / Photo: Jay Cronan

Delena cancerides collected at Mount Ainslie, ACT – March 2014
Source: Canberra Times
Photo: Jay Cronan

Research from Dr Rayor’s group suggests a lack of available habitat was the driving force for the evolution of sociality in these spiders. Their preferred habitat of tight spaces under peeling acacia bark is normally 80-100% occupied, so there’s not much room to spread out. The spiders are forced together due to a lack of available housing.

Social huntsman spiders aren’t attached to their family members; they only live together because there’s no other option. This is demonstrated when a colony has to move because their home is destroyed (usually the bark falling off the tree). The family doesn’t move as a group – the spiders go in search of new homes by themselves with no regard for their siblings and the small ones generally get eaten by predators.

These social spiders live (mostly) peacefully in family groups, but if there are big spiders trying to immigrate into their colony they will become aggressive and deny entry to the invaders (Beavis et al. 2007). This is consistent with the limited habitat concept as the spiders are protecting their home (a valuable resource). Young spiders don’t leave the family home until they are big enough to compete with others for the sparse housing options.

To test this idea the researchers looked at the relationship between the availability of suitable habitat and the occupants of the bark spaces. They found that as suitable habitat becomes rarer the number of spiders in each colony increases and there are more large spiders in the colonies (Yip 2012). In addition, the frequency of takeovers of bark spaces also increases when available habitat decreases.

Huntsman family

Delena cancerides siblings of varying ages sharing food / Photo: Linda Rayor

Instead of using a web to trap prey, huntsman spiders roam around at night and hunt their prey (hence the name ‘huntsman’). This food is brought back to the colony for consumption. Food is shared about 5% of the time – mainly between mothers and children and sometime older siblings even share with their younger brothers and sisters (Yip & Rayor 2013a). Even this small amount of sharing is very different to solitary spiders who share food less than 1% of the time.

Prey sharing means all the spiders in the group have some food often, so there is less variability in the amount of food they consume. This is very different to spiders living alone that can have erratic food availability. D. cancerides has a lower metabolic rate than solitary spiders which means they can survive on lower amounts of food (Zimmerman 2007). The researchers aren’t sure whether sociality arose because of the lower metabolic rate in these spiders or whether sociality allows them to share prey and they have developed a lower metabolic rate as a result – it’s a bit of a ‘which came first: the chicken or the egg?’ discussion in the research group at the moment.

It would be interesting to study the metabolic rate of some closely related social and solitary huntsman species to see if all social huntsman species have a low metabolic rate or just D. cancerides. This could possibly shed some light on the evolution of sociality in this group.

To learn more:

Click here to see Linda Rayor talking about social huntsman prey sharing dynamics and click here to learn about her field collection of spiders in Canberra this month.

Beavis AS, Rowell DM and Evans T (2007). Cannibalism and kin recognition in Delena cancerides (Araneae: Sparassidae), a social huntsman spider. Journal of Zoology, 271:2, 233-237.

Riechert SE and Lockley T (1984). Spiders as Biological Control Agents. Annual Review of Entomology, 29, 299-320.

Whitehouse MEA & Lubin Y (2005). The functions of societies and the evolution of group living: spider societies as a test case. Biological Reviews. 80, 347-361.

Yip E (2012). ‘Costs and benefits of group living in an unusual social spider, Delena cancerides’. PhD thesis, Cornell University, New York.

Yip EC & Rayor LS (2013a). The influence of siblings on body condition in a social spider: is prey sharing cooperation or competition? Animal Behaviour. 85, 1161-1168.

Yip EC & Rayor LS (2013b). Maternal care and subsocial behaviour in spiders. Biological Reviews, doi: 10.1111/brv: 12060

Zimmerman A (2007). ‘Assessing the Costs of Group Living: Comparing Metabolic Physiology and Growth in Social and Solitary Spiders’. PhD thesis, Cornell University, New York.