**5. Intra and interspecific transmission of bat viruses**

mechanisms. On the other hand, novel host defenses increase selection on the parasite. A tight genetic interaction between hosts and pathogens can lead to ongoing host-parasite coevolution, defined as the reciprocal evolution of interacting hosts and parasites [42]. The antagonistic coevolutionary arms race of parasite infectivity and host resistance leads to adaptations and counteradaptations in the coevolution and also has a central role in the evolution of host-parasite relationships in the microbial world [43]. A key consequence of coevolution is the impact on genetic diversity of host and parasite populations. The host-parasite coevolution is widely assumed to have a major influence on biological evolution by imposing a high selective pressure on both host and virus. Selected traits, genes involved, and the underlying selection dynamics represent central topics of interest for understanding host-parasite

The evolution of bats is a very successful singular history among mammals that have produced an enormous diversity of species with high mobility and great longevity adapted to a great spectrum of environments [42]. Bats host more zoonotic viruses and more total viruses per species than rodents, despite the fact that there is a lot more known species of rodents [45]. Furthermore, bats harbor a significantly higher proportion of zoonotic viruses than all other mammalian orders [46]. The antagonistic coevolutionary arms race of parasite infectivity and host resistance leads to adaptations and counteradaptations in the coevolution and also has a central role in the evolution of host-parasite relationships in the microbial world [47]. The origin of bats is estimated at about 64 million years ago or following the Cretaceous-Tertiary boundary [48]. The millions of years of bat evolution might have given rise to the coevolution processes between host and pathogen. The antagonistic coevolution between infectivity of viruses and resistance of bats is still poorly known. The ability of bats to harbor extremely lethal viruses for humans without apparent morbidity and mortality has long been discussed. The lack of abnormal ethology observed in virus-infected bats may be due at the selection of

The evolution of flight in bats has been accompanied by genetic changes to their immune systems to accommodate high metabolic rates. The increased metabolism and higher body temperatures of bats during flight might have enhanced their immune system, increasing resistance and thus increase the diversity of viruses they host [2, 49]. This increase of metabolic rate in bats is estimated to be 15- to 16-fold, when it is only sevenfold for running rodents and twofold for birds [2]. Marburg, Angola, Ebola, and Makona-WPGC07 viruses were shown to efficiently replicate at flight temperature of bats, i.e. 37 and 41°C, indicating that flight-related temporal elevation in temperature does not affect filovirus replication [50]. Furthermore, many bat species display a daily torpor with decrease of body temperature which might be a virus-resistance strategy, interfering with optimal virus replication [2]. Bats also display a unique interferon system (IFNs) that may explain the ability of bats to coexist with viruses [51]. Mammals have a large IFN locus comprising a family of IFN-α genes expressed following infection. Conversely, bats display a contracted IFN locus with only three functional IFN-α, but constitutively and permanently expressed [51]. This constitutive expression could turn to be a highly effective system for controlling viral replication and explain the resistance of bats to viruses. Differences have also been observed in the immune

coevolution [44].

120 Bats

resistance mechanisms.

Bats are considered major hosts for alphacoronaviruses and betacoronaviruses and they play an important role as the gene source in the evolution of these two genera of coronavirus [53]. Most, if not all, alphacoronaviruses and betacoronaviruses found in mammals are evolutionally linked to ancestral bat coronaviruses [54]. Different species of *Rhinolophus* bats in China carry genetically diverse SARS-like coronaviruses, some of which are direct ancestors of SARS-CoV and hence have the potential to cause direct interspecies transmission to humans [54]. A largescale study conducted worldwide on 282 bat species from 12 families demonstrated the presence of coronaviruses on 8.6% of bats whereas the ratio was only 0.2% on non-bat species [36]. A relationship between viral richness and bat species richness was demonstrated, suggesting that the diversity of bat CoVs has been driven primarily by host ecology [36, 41]. Preferred association between viral subclade and bat family was also observed. Bat-borne Dependoparvoviruses are also suspected to be the ancestral origin of adeno-associated virus (AAVs) in mammals [55]. Similarly, bats are the primary reservoir for 15 of 17 species of lyssaviruses [56]. Lyssaviruses may have evolved in bats long before the emergence of carnivoran rabies [6, 57].

Dissemination of viruses among bat populations is a complex system affected by many traits of the seasonal bats life. Seasonality and environmental conditions determine birthing periods, migrations, gregarious behavior, and torpor of each bat species. Each one may affect population density, rates of contact between individuals, and consequently the basic reproductive number of virus (R0 ) and virus transmission between species. The basic reproductive number (R0 ) is an important parameter in the dynamic of diseases and is the average number of new infections that would arise from a single infectious host introduced into a population of susceptible hosts [58]. Understanding how pathogens spread within their host populations is a key factor in epidemiology. It is especially difficult to study the vertical transmission of viruses in bats. Bats are very sensitive to disturbances and environmental changes, especially during breeding period. A disturbance in a maternity colony can produce an important mortality in newborn bats that may impact in the demography of population. The per capita transmission rate depends on the infectivity of the virus, the susceptibility of the host, but also on the contact rate between susceptible hosts and infectious individuals. Social organization within the refuges thus plays a major role in virus transmission. Some bat species form a very large and tight monospecific or multispecific colonies of thousands individuals, e.g. the density of a hibernation colony of *Miniopterus schreibersii* near Barcelona was estimated at 1900 bats for square meter [58] (**Figure 4**). *Tadarida brasiliensis Mexicana* forms in Carlsbad Cavern (New Mexico), a colony with 793,838 bats [59]. This gregarious roosting behavior can provide large opportunities for viral exchange in bat colonies. Bat colonies are often composed by more than one species. Large colonies and multispecies associations are frequent among cave-dwelling bats, in particular during the maternity period. This colonial behavior confers thermodynamic and social advantages to reproductive females during pregnancy and lactation [60]. For instance, mixed colonies can be found in Southeastern Europe where *Miniopterus schreibersii*, *Myotis myotis*, and *Myotis capaccinii* are in direct physical contact. This cohabitation can facilitate virus transmission between species. The seroprevalence for EBLV-1 in *Myotis myotis* and *Miniopterus schreibersii* followed the same temporal pattern during 4 years [45], which could be explained by virus transmission between these two species. The size of the colony and species richness were two important ecological factors playing a major role in seroprevalence variability [45]. Virus transmission in colonies may follow different ways depending on the bat and virus species considered, i.e. aerosols, contact with feces, urine, blood, or other body fluids, or by bite. Ectoparasites should also be considered. There are almost no data on vertical transmission from mother to fetus. However, vertical transmission has nevertheless been reported. Transplacental transmission of Hendra virus (HeV) was shown in the fruit bat *Pteropus poliocephalus* [61]. Horizontal transmission is far more documented. Theoretical modeling of disease expansion has assumed large and well-mixed host populations. However, many wildlife systems have small groups with limited contacts among them. The distribution of seropositive bats against European Bat Lyssavirus type 1 (EBLV-1) is not random in bat colonies and follows a gregarious pattern, indicating a non-random transmission of viruses inside the colony. Most of gregarious species of bats have a metapopulation structure (consisting of periodically interacting, spatially discrete subpopulations) with variations in their subpopulations. The total number of individuals in the various subpopulations must be sufficient to maintain virus circulation in the metapopulation over time, while immunity or death due to viral infection extinguishes transmission chains within individual subpopulations. In a longitudinal study in vampire bats of Peru, Blackwood et al. [62] found that persistence of rabies virus cannot occur in a single colony. Maintenance of rabies virus at levels consistent with field observations requires dispersal of bats between colonies, combined with a high frequency of immunizing non-lethal infections. The dynamic of virus infection in a bat colony usually produce periodic oscillations in the number of susceptible, immune and infected bats. The delay between the waves depends upon the rate of inflow of susceptible bats into the colonies as a consequence of new births, immigration of naïve animals from neighboring colonies, and expiration of immunity in previously infected animals. When a sufficient fraction of susceptible individuals in the bat population is reached, the virus spreads again if infected individuals joined the colony [63]. A high number of species might not only increase the rate of contact between bat groups and species but also could facilitate virus entry or spread through the higher mobility of individuals among colonies, especially if these bats exhibit a migratory behavior. The role of migratory species in virus dispersion is unfortunately poorly studied in spite of being very important.

Bats, Bat-Borne Viruses, and Environmental Changes http://dx.doi.org/10.5772/intechopen.74377 123

**6. Anthropization, human behavior, and dynamic of emergence**

ior, landscape evolution, and anthropization.

The main element for the emergence of an infectious disease is the contact. With no contact, there is no possibility for a virus to cross the species barrier. In the case of bat-borne diseases, a direct or indirect contact must occur for the disease to emerge and spread. Synanthropic bats are of course the first ones to be considered as a source of emerging viruses. However, they are far from being the only ones at risk for transmission to humans. It is not only the natural synanthropic behavior that matters but instead the whole complex of biology, ecology, behav-

The first interaction considered for transmission of bat-borne viruses to humans is hunting and consumption of bush meat [64]. This is a traditional interaction in which humans are potentially going towards bats and thus viruses. However, there is no documentation of direct origin of virus disease outbreak coming from bat hunting, butchering, and consumption. Bush meat has been for instance regularly considered for the emergence of Ebola [65]. However, there is no evidence of direct contact with bats and bats were not the primary bush meat. Bats might just be a reservoir involved in a sylvatic cycle involving other animals being the actual target of bush hunting. In places where bats are hunted and consumed such as Southeast Asia, there is no report of direct emergence of viral diseases coming from consumption or hunting. A more likely potential process of transfer of viruses from bats to humans might be the attractiveness of degraded environment for bats [41]. Indeed, a highest diversity of bat-borne viruses was demonstrated, as a consequence of a higher diversity of bats, in anthropized, degraded environments. Deforestation and anthropization, instead of leading to the elimination of bats as one would instinctively expect, generate conversely a higher diversity. This might be explained by the complexity of the anthropized environments, which offer opportunities to different groups

**Figure 4.** Colony of *Miniopterus schreibersii* with individuals tightly close to each other.

circulation in the metapopulation over time, while immunity or death due to viral infection extinguishes transmission chains within individual subpopulations. In a longitudinal study in vampire bats of Peru, Blackwood et al. [62] found that persistence of rabies virus cannot occur in a single colony. Maintenance of rabies virus at levels consistent with field observations requires dispersal of bats between colonies, combined with a high frequency of immunizing non-lethal infections. The dynamic of virus infection in a bat colony usually produce periodic oscillations in the number of susceptible, immune and infected bats. The delay between the waves depends upon the rate of inflow of susceptible bats into the colonies as a consequence of new births, immigration of naïve animals from neighboring colonies, and expiration of immunity in previously infected animals. When a sufficient fraction of susceptible individuals in the bat population is reached, the virus spreads again if infected individuals joined the colony [63]. A high number of species might not only increase the rate of contact between bat groups and species but also could facilitate virus entry or spread through the higher mobility of individuals among colonies, especially if these bats exhibit a migratory behavior. The role of migratory species in virus dispersion is unfortunately poorly studied in spite of being very important.
