Ecological and Evolutionary Perspectives on Transmissible Viral Tumours in Wild Species

A. Garcês*, I. Pires and F. Silva

Andreia GARCÊS*, DVM, MSc, PhD, Exotic and Wildlife Service at the University of Tras-os-Montes and Alto Douro; Centre for Research and Technology of Agro-Environmental and Biological Sciences, CITAB, Inov4Agro, University of Trás-os-Montes and Alto Douro; CECAV, University of Tras-os-Montes and Alto Douro, Vila Real, Portugal (Corresponding author, e-mail: andreiamvg@gmail.com); Isabel PIRES, DVM, MSc, PhD, CECAV, Portugal; Filipe SILVA, DVM, MSc, PhD, CECAV, University of Tras-os-Montes and Alto Douro, Vila Real, Portugal

https://doi.org/10.46419/vs.56.1.9

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Abstract

An oncogenic virus is a virus that has the potential to cause cancer. These viruses can induce the malignant transformation of cells by various mechanisms, such as integrating their genetic material into the host cell’s genome or by expressing viral proteins that interfere with normal cellular processes. Understanding and monitoring oncoviruses in wildlife is essential for wildlife conservation efforts. This review aims to provide an overview of oncoviruses of veterinary importance in wild animals and their ecological and evolutionary perspectives on transmissibility. These viruses can contribute to declines in population numbers and alter the dynamics of ecosystems. Conservation biologists and veterinarians work to study and manage these diseases to mitigate their impact on wildlife populations.

Key words: oncogenic; virus; tumours; wild-life

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Introduction

An oncogenic virus is a virus that has the potential to cause cancer (Mui et al., 2017). The first animal oncovirus discovered was the “Rous sarcoma virus (RSV)”, a retrovirus identified by American virologist Peyton Rous in 1911. Peyton Rous made this groundbreaking discovery while working with sarcomas (cancers of connective tissues) in chickens (Rous, 1910). Several viruses are known to be oncogenic and classified into two main groups: DNA viruses and RNA viruses (Tempera and Lieberman, 2021). Oncogenic viruses can be divided into direct and indirect oncogenic viruses (Elkhalifa et al., 2023). Direct oncogenic viruses contribute directly to neoplastic cellular transformation, while indirect oncogenic viruses cause chronic inflammation that can lead to tumour development (Elkhalifa et al., 2023).

These viruses can induce malignant cell transformation by various mechanisms. It is important to note that while these viruses can increase the risk of cancer, not every animal infected with an oncogenic virus will develop cancer, and even if it develops, it can take years before the first signs appear. Other factors, including the individual’s immune response and genetic predisposition, also play a role in cancer development (Xie et al., 2004; Tempera and Lieberman, 2021).

Cancer has been recorded in almost every group of animals, and there is significant variability in the nature and incidence of tumours among species. This disease is a significant factor in morbidity and mortality among various wildlife species. Wildlife cancer detection can be complex; in most cases, it goes largely undetected (McAloose and Newton, 2009).
Difficulty in accessing animals (dead or alive), whether due to environmental obstacles (e.g. oceans, deserts, jungles), species-specific adaptations (e.g. deep dive), decomposition, predation or scavenging, or a lack of resources in the field, both human and financial, hinder cancer detection in these populations (Acevedo-Whitehouse and Duffus, 2009; McAloose and Newton, 2009). However, wildlife health monitoring has been increasing in recent years, providing new epidemiological and alarming information concerning the presence and impact of cancer in wildlife populations (McAloose and Newton, 2009).

Oncoviruses are not limited to human populations or domestic animals; they can also affect various wildlife species. In the wild, oncoviruses have been identified in different animals, and these infections can contribute to developing cancers in those species (Parisi et al., 2023). Wildlife oncoviruses can be a significant concern for conservation efforts, as they may impact the health and survival of vulnerable populations (McAloose and Newton, 2009; Mui et al., 2017; Frias-De-Diego et al., 2019). Cancer has become a threat to already endangered populations such as the Western Barred Bandicoot (Perameles bougainville) or Loggerhead Turtle (Caretta caretta) (McAloose and Newton, 2009).
This review gives an overview of the most common oncoviruses of veterinary importance in wild animals and their ecological and evolutionary perspectives on transmissibility.

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Oncoviruses in wildlife

Several viruses have been identified as oncoviruses (e.g. Papillomaviridae, Herpesviridae) and are associated with various types of animal cancers (Mui et al., 2017). Here, the authors describe some examples of oncoviruses from different virus families:

Papillomaviridae

Papillomaviruses in wildlife
Papillomaviruses (PV) are small, unenveloped DNA viruses known to produce lesions on the skin and mucous membranes (fibropapillomas and papillomas) of various species, including humans (Araldi et al., 2017; Frias-De-Diego et al., 2019; Rector and Van Ranst, 2013).
The PV family has 26 genera, 62 species and 69 known animal Pvs with high genetic variability (Table 1).

Table 2. Oncogenic viruses are present in wildlife. — **Table 1**. Oncogenic viruses are present in wildlife.

Each papillomavirus species tends to be specific to a particular host species or a closely related group (Humans, 2007; Rector and Van Ranst, 2013). PV has been reported in several wild animals such as Camelus dromedarius, Alces alces, Capreolus capreolus, Lynx rufus, Phocoena phocoena, Macaca fascicularis, Trichechus manatus latirostris or Morelia spilota spilota (Table 1) (Rector and Van Ranst, 2013). Skin warts are the most common sign of infection with PV.

They are usually benign tumours in the skin, but can be malignant when they develop in the genital tract. PV replicates exclusively in keratinocytes (Lambertsen et al., 1987; Araldi et al., 2017;). The most common macroscopic manifestation of PV infections is the development of warts or papillomas that are raised, rough, and well-demarcated growths on the skin or mucous membranes. They may be small, discrete papules or larger, cauliflower-like structures with multiple finger-like projections and white rough or verrucous texture (Vengušt and Žele, 2012). The colour may be flesh-coloured, pink, brown, or hyperpigmented, depending on the skin pigmentation and inflammation (Garcês et al., 2020). The lesions can be solitary or multiple, and common growth sites include the hands, feet, face, genital, perianal regions, and mucous membranes (De Guise et al., 1994; Rector and Van Ranst, 2013; Frias-De-Diego et al., 2019). They may ulcerate and bleed. Histopathological characteristics can vary depending on the type of papillomavirus, the host species, and the specific tissue involved. It is possible to observe hyperplasia, koilocytosis, acanthosis, papillomatosis, parakeratosis, dysplasia, mitotic figures and inflammatory response (Figure 1).

**Figure 1**. A – Skin fibropapilloma (4x3x3 cm) in Red Deer (*Cervus elaphus*). B – The presence of koilocytes in the spinal stratum and images suggest intranuclear basophilic inclusions in a skin fibropapilloma in Red Deer (*Cervus elaphus*) (Photo Andreia Garcês/Isabel Pires).

Transmission of PV requires close cutaneous or mucosal contact with microtraumas in the skin or mucosal surface (Rector and Van Ranst, 2013). Transmission from infected females to susceptible calves through skin contact during suckling or from males to females during breeding is also possible (De Guise et al., 1994; Humans, 2007; Rector and Van Ranst, 2013). Studies also show that the virus can be transmitted by flies and ticks (Araldi et al., 2017).

Herpesviridae

Urogenital carcinoma in wild California sea lions
Around 18–23% of adult animals in wild California Sea Lion (Zalophus californianus) populations examined post-mortem over the past 40 years displayed urogenital carcinomas (Gulland et al., 2020).
The aetiology of this malignant neoplasia remains poorly understood, but researchers believe it is multifactorial, with pollution (organochlorines and polychlorinated biphenyls), genotype and infection with Otarine herpesvirus-1 (OtHV-1) as possible agents (King et al., 2002; Gulland et al., 2020). Figure 2 represents the distribution of OtHV-1 worldwide.

**Figure 2**. Green the distribution of OtHV1 in California sea lion (*Z. californianus*) (Author: Andreia Garcês).

Primary tumours occur in the cervix, vagina, penis, or prepuce and aggressively metastasise, resulting in death (Venn-Watson et al., 2012; Deming et al., 2021) vagina, penis, or prepuce and aggressively metastasize resulting in death. This cancer has been strongly associated with a sexually transmitted herpesvirus, otarine herpesvirus 1 (OtHV1). The presence of thickened and dysplastic mucosal epithelium characterises the histological lesions.
Distinct cytoplasmic borders, polygonal to round cells with moderate amounts of cytoplasm, squamous cell differentiation/keratinisation are present and, in some females, glandular differentiation.
Intranuclear inclusion bodies were identified in primary neoplasia and metastatic lesions (abdominal and pelvic lymph nodes, kidney, urinary bladder, liver, lungs and spleen) (Browning et al., 2015).
Cytokeratin positivity confirms tumour epithelial ontogeny (Newman and Smith, 2006a; Deming et al., 2018;).

Pollution has already been associated with other tumours, such as the gastric papilloma in the St Lawrence River’s Beluga (Delphinapterus leucas) (De Guise et al., 1994). Studies showed that blubber from sea lions with urogenital carcinoma had significantly higher levels of polychlorinated biphenyls and DDTs than blubber from healthy sea lions without carcinoma (Newman and Smith, 2006a; Deming et al., 2018).

OtHV1 is a gammaherpesvirus in the genus Rhadinovirushas. Electron microscopy, immunohistochemistry, and polymerase chain reaction (PCR) studies have shown the presence of herpesvirus in affected animals (Buckles et al., 2006; Newman and Smith, 2006b). OtH-1 is more prevalent in adult tissue than in juveniles.
The virus has been associated with sexual transmission, and Deming et al. (2021) identified that non-cancer OtHV1-positive cases had significantly lower viral loads in their cervix compared to the cervix of animals with urogenital carcinoma (Deming et al., 2021). Vertical transmission during pregnancy or birth has been suggested to introduce OtHV1 to new individuals. Infected mothers may pass the virus to their offspring, contributing to the persistence of the virus in the population (Buckles et al., 2007). Two potential oncogenes were identified in OtHV-1, the viral B-cell lymphoma 2 gene (vBCL2) and viral Fas-associated death-like interleukin-1 beta-converting enzyme-inhibitory protein (vFLIP). Both genes are of host origin and are observed in other gamma-herpesviruses that induce cancer in humans and animals by preventing apoptosis during cell division.

Genetic predisposition to cancer also is possible, as these carcinomas are more common in relatively inbred individuals (Acevedo-Whitehouse et al., 2003).
OtHV1, like other herpesvirus, often exhibits latency, where the virus remains dormant within the host cells. Stressors, such as changes in the environment, competition, or compromised immune function, can trigger the reactivation of the virus, leading to shedding and potential transmission (Venn-Watson et al., 2012; Deming et al., 2021).

Retroviridae

Koala retrovirus
The koala (Phascolarctos cinereus) population is affected by a virus-denominated koala retrovirus (KoRV) (Figure 3).

**Figure 3**. Distribution of koala retrovirus (KoRV) and bandicoot papillomatosis carcinomatosis virus type 1 (BPCV1) (Author: Andreia Garcês).

KoRV belongs to the family Retroviridae, genus Gammaretrovirus, and the virions contain a positive-sense single-stranded RNA genome of 8,431 nucleotides in length (Xu and Eiden, 2015). This virus is relatively recent and has become endogenous and fixed in the genome of every koala cell, and it is transmitted vertically (Zheng et al., 2020). KoRV has been divided into three major clades and nine subtypes (KoRV-A to KoRV-M) based on sequence differences in the receptor binding domain of the envelope protein gene. The virus has shown high homology with the Gibbon Ape Leukaemia Virus (GALV) (Xu and Eiden, 2015).

Most koalas found positive for KoRV do not have clinical signs of the disease.
KoRV-G, KoRV-H, and KoRV-I subtypes have been identified in diseased wild Australian koalas (Stephenson et al., 2021). This virus is associated with the development of lymphoid neoplasia, and in northern koalas (lymphoma and leukaemia), some exogenous subtypes have been associated with more severe chlamydiosis (Stoye, 2006).

Bandicoot papillomatosis carcinomatosis virus

The Western Barred Bandicoot (Perameles bougainville) population has been affected by cutaneous and mucocutaneous papillomatosis and carcinomatosis syndrome in both captive and wild individuals. Bandicoot papillomatosis carcinomatosis virus type 1 (BPCV1) is the cause of this disease (Figure 3). BPCVs are double-stranded DNA viruses and are founding members of a novel virus family. Histological, ultrastructural, and immunohistochemical analyses have shown the involvement of papillomavirus (PV) or polyomavirus (PyV) in the pathogenesis of this disease (Bennett et al., 2008b) tentatively named bandicoot papillomatosis carcinomatosis virus type 2 (BPCV2. A case of BPCV-2 infection in a Southern Brown Bandicoot has been detected (Bennett et al., 2008b).

Clinically, the lesions appear as irregular thickenings and masses in the skin of the digits, body, pouch, mucocutaneous junctions of the lips, and conjunctiva (Woolford et al., 2008). Lesions can lead to difficulties in vision, locomotion, and ability to feed, depending on the anatomic location of the lesions. The lesions may also become abraded, ulcerated, and secondarily infected, leading to sometimes fatal complications. Metastases have been observed in lymph nodes, lungs, and the liver (Bennett et al., 2008a; Woolford et al., 2007, 2008).

BPCVs appear to be species-specific.
Transmission between individuals can occur through direct contact (e.g., mating, territorial fighting, and foraging behaviour) or vertically (from parents to offspring). While less common, transmission through fomites (inanimate objects or surfaces) contaminated with the virus is possible (Woolford et al., 2007; Bennett et al., 2008a).

Polyomaviridae

Polyomavirus in raccoons
Raccoon polyomavirus (RacPyV) is one of the most recently discovered members of the Polyomaviridae family (Figure 4).

**Figure 4**. Distribution of Raccoon polyomavirus (RacPyV) (Author: Andreia Garcês).

RacPyV was found 2010 in North American free-ranging raccoons (Dela Cruz et al., 2013). Polyomaviruses have a circular double-stranded DNA genome. The genomic structure of RacPyV includes genes that encode viral proteins, and its genome is organised into early and late regions (Giannitti et al., 2014; Lu et al., 2017).

RacPyV causes asymptomatic or mild infections (respiratory and gastrointestinal), but in some cases, they have been associated with the development of tumours. This virus has been associated with malignant peripheral nerve sheath tumours and undifferentiated sarcomas (Giannitti et al., 2014). Metastases have only been reported in a single case (Pesavento et al., 2018). Studies suggest that the target cell of virus transformation is the multipotent neuroglial stem cells of the brain’s subventricular zone (Church et al., 2016; Pesavento et al., 2018).

The precise mode of transmission remains unknown. It is thought to be transmitted through the oral-faecal route and possibly through respiratory secretions (Giannitti et al., 2014; Church et al., 2016).

Table 1 lists oncogenic viruses present in wildlife, their host, type of tumour and virus strain.

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Ecological and Evolutionary Perspectives

From an ecological perspective, transmissible oncovirus can significantly impact the population dynamics of an affected species.

The spread of the tumour can lead to population decline or altered age structures within populations. It may induce changes in the behaviour of affected individuals, for example, alterations in mating performances or social interactions (Hahn, 2002).
Habitat structure, host density, and interactions between infected and uninfected individuals affect disease transmission (Mui et al., 2017; Tempera and Lieberman, 2021). These alterations have already been observed in species such as the Eurasian Red Squirrel (Sciurus vulgaris) (Shuttleworth et al., 2022) or Western Barred Bandicoots (Perameles bougainville) (Woolford et al., 2007), whose populations are in decline due to the high prevalence of tumours caused by a virus.

Another example is the FeLV infection in wild felids, some already very threatened species, due to contact with domestic cats. Outbreaks in these populations could have disastrous consequences.
Studies suggest that changes in the environment, like the introduction of artificial feeders, may increase the contact among lynxes and between lynxes and other species, raising the risk of FeLV transmission (Luaces et al., 2008; Tangsugjai et al., 2010). This finding implies that conservation plans should carefully consider any interventions that might inadvertently increase disease risks.

From an evolutionary perspective, the coevolutionary dynamics between the host and the transmissible tumour are of interest since they raise questions about how the host’s immune system responds to the cancer cells and how they evolve to evade the immune system. The genetic diversity within host populations also may influence susceptibility to transmissible tumours, therefore, understanding the genetic basis of resistance or susceptibility can provide insights into the evolutionary processes at play (Mui et al., 2017;Te mpera and Lieberman, 2021).

Transmissible tumours can have profound evolutionary consequences. If the disease leads to the decline or extinction of a population, it can impact the genetic diversity of the species and, consequently, its evolutionary potential. The cancer cells themselves may undergo adaptive changes to enhance their transmission.
Understanding the genetic mechanisms that facilitate transmission is essential to comprehend the evolutionary dynamics of these diseases (Pesavento et al., 2018; Tempera and Lieberman, 2021).

Comprehensive disease control programmes that encompass prevention and eradication are necessary. However, implementing such programmes is often challenging due to limited data, high costs, and logistical difficulties. The study by López et al. (2009) on managing an FeLV outbreak in Iberian lynxes is a relevant example. The plan aimed to conduct serological surveys, isolate infected lynxes, vaccinate uninfected ones, and control feral and domestic cat populations.
The outbreak was successfully contained within eight months, and over 80% of the lynx population was vaccinated.

It is urgent to focus on assessing pathogen risks, prioritising surveillance and control strategies, and understanding the role of domestic reservoirs and environmental factors in disease outbreaks.
Proactive planning and preparedness are crucial to protect endangered species from potentially devastating disease outbreaks (López, 2009).

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Conclusions

It is important to note that the relationship between viruses and animal cancers can vary. In some cases, the association is well-established, while in others, the role of the viruses in cancer development is still poorly studied.
Additionally, just as in humans, the development of cancer in animals is likely influenced by a combination of factors, including genetics, the immune system, and environmental factors.

Research on oncoviruses in animals is essential for understanding the mechanisms of cancer development and developing strategies for prevention and treatment. Veterinary medicine and wildlife conservation efforts often focus on monitoring and managing the impact of oncoviruses on animal health.

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Acknowledges

The participation of Pires I, Garcês A., Silva F. was supported by the projects UIDB/CVT/00772/2020 and LA/P/0059/2020, funded by the Portuguese Foundation for Science and Technology (FCT). (Pro-ject UIDB/CVT/0772/2020). The participation of Garcês A. was supported by National Funds from FCT Portuguese Foundation for Science and Technology, under the project UIDB/04033/2020.

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Ekološke i evolucijske perspektive na prijenosne virusne tumore u divljih vrsta

Andreia GARCÊS, DVM, MSc, PhD, Exotic and Wildlife Service at the University of Trasos-Montes and Alto Douro; Centre for Research and Technology of Agro-Environmental and Biological Sciences, CITAB, Inov4Agro, University of Trás-os-Montes and Alto Douro; CECAV, University of Tras-os-Montes and Alto Douro, Vila Real, Portugal; Isabel PIRES, DVM, MSc, PhD, CECAV, Portugal; Filipe SILVA, DVM, MSc, PhD, CECAV, University of Tras-os-Montes and Alto Douro, Vila Real, Portugal

Onkogeni virus je virus koji potencijalno može prouzročiti rak. Ti virusi mogu izazvati malignu transformaciju stanica različitim mehanizmima, poput integriranja njihovog genetskog materijala u genom stanice domaćina ili ekspresijom virusnih proteina koji ometaju normalne stanične procese. Razumijevanje i nadziranje onkovirusa u divljih životinja od osnovne je važnosti u naporima za očuvanje divljih životinja. Ovaj pregled ima za cilj pružiti prikaz onkovirusa od veterinarske važnosti u divljih životinja i njihove ekološke i evolucijske perspektive na prijenosne virusne tumore. Ovi virusi mogu doprinijeti smanjenju populacije i izmijeniti dinamiku ekosustava. Konzervacijski biolozi i veterinari rade na proučavanju i upravljanju ovim bolestima kako bi se ublažio njihov utjecaj na populacije divljih životinja.

Ključne riječi: onkogeno, virus, tumori, divlje životinje

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