List
of Abbreviations
GWAS Genome
wide association studies
RHM Regional
heritability mapping
SNP Single
nucleotide polymorphism
QTL Quantitative
trace loci
INTRODUCTION
The major hindrance to profitable and sustainable
livestock production in sub-Saharan Africa is the high prevalence of ticks and
the diseases they transmit known as tick-borne diseases. The burden is also
high in other tropical and subtropical areas outside of the African continent.
The losses have been felt from way back into time, with reports of an estimated
loss of US$186 million due to East Coast Fever alone in the year 1989 in over
10 countries in sub-Saharan Africa (Dolan 1999). As recent at 2021, Zimbabwe has seen increases in
morbidity and mortalities of cattle, due to tickborne
diseases, mainly theileriosis (Nhokwara et al.,
2023).
Several methods of controlling ticks and consequently tickborne diseases have been used before. The main method
used in sub-Saharan Africa is the use of chemicals called acaricides
which kill the ticks. Other methods used in the control of ticks, albeit at a
smaller scale are biological control methods, tick vaccines and pasture and
grazing management. Pasture spelling has been done with fair results in some
countries as the method only works against certain tick species such as Rhipicephalus (Boophilus) microplus which cattle are the exclusive host (Deken, et al. 2010). Anti-tick vaccines are still largely in the
development phase, they gave satisfactory immunity but had to be administered a
number of times in a year and needed to be combined with acaricide
application for full efficacy. Furthermore they have not been widely adopted in
the needy regions of East, Central and Southern Africa. (Kasaija, et
al., 2023).
The traditional method of using acaricides
to control ticks has become unsustainable due to the high costs of purchasing acaricides coupled with increasing reports of tick
resistance to the chemicals. This presents a huge problem to the livestock
sector as the high acaricide costs increase input
costs in livestock production and also it takes time for new effective
chemicals to be developed (Deken, et al. 2010). Furthermore, there is an important issue of the
development of ticks that are resistant to these chemicals. These strains
evolve at a faster rate than the development of any new chemical, (Kemp et al,
1999) leaving the farmer with chemicals that are increasingly becoming
ineffective. All these challenges have an even greater negative effect on the
livelihoods of communal farmers that depend on livestock.
Adding on to
that, chemical control of ticks has always been criticized for its negative
impact on the environment. Chemicals such as arsenic compounds and pyrethroids (which is now the predominant dipping
chemical), have all been reported to have varying consequences such as arsenic
poisoning of oxpeckers (Buphagus species) which threatens
them with extinction (Livestock Production Program/Animal Health Program, 2003).
The best solution to the challenges of conventional tick
control methods may lie in the identification and use of animal breeds that are
naturally resistant to ticks. (Hayward 1981). Tick resistance can be defined as
an animal's ability to limit the number of ticks that develop on it to maturity
(Utech et al, 1978). Although the environment also
plays a role, genetics still bear a significant part of an animal's disease
resistance ability (Spickett et al., 1989; Rechav et., 1991). The numbers of ticks that infest cattle show a huge variation, largely believed to be due
to the genetic makeup of the host. Several studies have demonstrated that even
under the same ecological environment, some breeds of cattle are infested by
fewer ticks than do others
(Latif, et al., 1991; Marufu et al., 2011) with much of these differences due to
the host animal's immunological response to infestation.
Impacts of ticks and tickborne
diseases
Ticks are vectors of
several major diseases of cattle and also cause other minor ailments, all
leading to production losses. Bites from ticks irritate, sometimes leaving
wounds that predispose the host animal to screw-worm myiasis,
and expose it to other bacterial and fungal pathogens (Bram & George, 2000). In addition, livestock owners also lose
due to the costs implicated in treatment, prevention and control efforts.
Globally, tick-borne
diseases are among the most important causes of production losses for beef and
dairy cattle with estimated losses upwards of
US$22 billion per year (Tabor, et al., 2017). The tropical and
subtropical regions suffer the biggest losses from tickborne
diseases than other regions of the world
(Estrada-Pena & Salman, 2013). Although there are dozens of tickborne diseases, only a handful are of major economic
importance. These diseases are caused by different etiological agents such as
protozoa and bacteria, affecting different systems in the body such as the
circulatory system and lymphatic system, but are all transmitted by ticks (Jongejan,
2004). The major tickborne diseases affecting
tropical cattle will now be briefly discussed below.
Bovine
Babesiosis
Babesiosis, also known as redwater or tick fever, is a disease of animals characterised by a fever, anaemia,
haemoglobinuria and icterus. It is caused by intra-erythrocytic parasites of the Babesia
species transmitted by a number of tick species (Taylor et al. 2004). In sub-Saharan Africa, the
most important species are Babesia bigemina and B. Bovis transmitted by Rhipicephalus (Boophilus) decoloratus and R.(B). microplus respectively (Urquhart et
al., 2007). The exotic European breeds of cattle are more susceptible,
although the Zebu and Sanga are also affected. The
acute disease manifests via a high fever (above 40°C), inappetance
and a reluctance to move. Anaemia and haemoglobinuria ( hence the name redwater) follow in prolonged cases with fatalities common
as well. Cerebral babesiosis occurs in B. bovis infections,
with additional signs such as hyperesthesia, head pressing, cycling and
convulsions. Chemotherapy with a number of drugs is crucial in clinical cases
of babesiosis, and the success thereof hinges on
early diagnosis and prompt drug administration. The common prevention method is
by controlling the tick vectors by regular dipping of cattle with acaricides at intervals, usually of two weeks or less (Vos et al. 1996).
Bovine
anaplasmosis
Bovine anaplasmosis (or gall sickness) is an infectious,
noncontagious arthropdod borne disease of cattle
caused by the rickettsial organisms, Anaplasma marginale and
A. centrale.
The disease is widespread around the world and several tick species are known
to biologically transmit the causative organism while some biting flies such as
those of the Tabanidae family transmit mechanically (Urquhart, et al. 2007). Clinically, Anaplasmosis is characterized by fever, anaemia,
weakness, constipation, icterus and laboured breathing. It also causes production losses due to
reduced meat or milk production as animal's recover slowly if they survive
acute infection (Drummond 1983) The
disease is treated by a combination of drugs, and success also depends on
prompt diagnosis and administration of the correct drugs. Prevention is largely
by control of tick vectors although a vaccine made from the A. centrale isolates
is available with varying results obtained around the world.
Heartwater
Heartwater is a septicaemic, often fatal, disease of ruminants. The
causative organism is Ehrlichia ruminantium, a bacteria which is transmitted by ticks of the genus Amblyomma (Allsop, 2015).
The disease is enzootic in sub-Saharan Africa, the areas corresponding to the
distribution of the vector species. It has also been reported in the Carribean islands following cattle imports (Allsop, 2015). The peraute
forms of the disease cause sudden deaths and acute forms are characterized by
central nervous system signs such as cycling, head pressing and ataxia.
Treatment can result in recovery if given early. Vaccination with blood based
vaccines is common in enzootic areas although control of the disease still
mainly relies on dipping of cattle with acaricides (Meltzer, Perry, & Donachie, 1996).
Theilerioses
These are diseases
caused by the tick-transmitted protozoa, Theileria parva in east and southern Africa. In North Africa, Asia
and southern Europe, Theileria annulate
is the causative agent. In its classical form, the disease causes severe
clinical signs and fatalities. The tick vector is the brown ear tick, Rhipicephalus appendiculatus.
The different disease syndromes caused by this parasite are East Coast fever, January
disease (Zimbabwe Theileriosis) and Corridor disease.
The clinical signs are typically fever, swelling of lymph nodes, laboured breathing, sometimes corneal opacity and bloody diarrhoea ending in death
(Lawrence, Perry, & Williamson, 1996). Chemotherapy is used in clinical cases
although success is largely dependent on early diagnosis and instituting
treatment. The infection-treatment method has been used in vaccinations using a
vaccine developed in East Africa, the so-called Muguga
cocktail. However, acaricide application for tick
control is still the main method for controlling the disease with application
being done as frequently as less than seven days to control outbreaks.
Conventional tick control methods and their challenges.
Traditionally, ticks
have been controlled by the application of chemicals, called acaricides, onto the host animal. The costs involved in
this have been a huge burden on the livestock sector. These chemicals often
have to be applied every week or every fortnight, depending on the strategy in
use. There are also infrastructure development and equipment maintenance costs
involved as well. Various methods of application of these chemicals have been
used, from dipping tanks to spray-races and hand-dressing. They all have their
own merits and demerits such as their efficacy in killing the ticks and the
cost of setting up. Thus farmers have the choice to select a preferred method
based on their farm circumstances (Deken, et al. 2010).
The use of dipping
tanks is a very effective method in tick control as there is usually full
immersion of the animal and all tick predilection sites are reached by the
chemical. However, they have a high initial cost of setting up, making them out
of favour by small-scale farmers unless it's a
collective effort, usually led by a government agency. Hand spraying has become
a common acaricide application method in the
smallholder sector due to the high costs of building dipping tanks. The method
has several disadvantages, mainly around inadequate application of chemicals
and failure to reach the relatively inaccessible areas on the animal's body
such as the ears and axilla. Spray races offer a cheaper alternative to the
dipping tank (Deken, et al. 2010). They
use many nozzles that try to reach as many parts of the animal as possible.
Usually, they have a motor-driven pump that generates high pressure reaching
the whole body. They also use smaller amounts of acaricide
than the dipping tank. Hand dressing of acaricide is
usually done as an emergency and/or complementary method to any of the above
methods. It targets particular areas on the animal's body where particular
ticks or tick stages are known to habitat. This is usually very effective in
eliminating particular ticks.
To add onto the costs
of setting up, running and maintaining an acaricide
application program, there is another developing, more worrying challenge of acaricide resistance. The genetic selection of acaricide-resistant tick strains has become a major drawback
to tick control by acaricides. Tick resistance to acaricides can be defined as a tick strain's ability to
tolerate acaricide doses that normally kill the
majority of the ticks in a population of that very species (Deken, et al. 2010). It is an evolutionary
adaptation due to certain physiological mechanisms in the resistant ticks (Waldman, Klafke, & Jr, 2023). In any given
population of ticks, there are always some individual ticks that can better
withstand the effects of acaricides but this
resistance is not always inherited by their offspring. However, survival
against acaricide treatment by these individuals
selects only them, and their reproduction increases the proportion of resistant
individuals thus spreading the genetic acaricide resistance (Deken,
et al. 2010). The acaricide acts
as a selective screening process which leaves only the acaricide-resistant
individuals that were already present in a population. Acaricide
resistance is a process that takes several generations of ticks in a given population.
Concentrations of acaricide that truly do not kill
any ticks, do not select for resistance as all individuals will survive, and
those that are lethal to all ticks do the same. So the development of
resistance occurs at some point in between, where some individuals survive
while others die as illustrated in Figure 1.
These resistant
strains often evolve at a faster rate than any new chemical can be developed ( Kemp et al, 1999). Wharlton
& Roulston, (1970) reports that resistance of the tick species Rhipicephalus (Boophilus) decoloratus and Rhipicephalus (Boophilus) microplus can now
be expected within a decade of the introduction of a new acaricide.
The situation is dire especially with these species because they are one host
tick that spend about 23 days of their life cycle attached to the animal's body
(Wharlton
& Roulston, 1970), exposing them and their offspring to many acaricide treatments when regularly done say every seven
days. With three host ticks like the Rhipicephalus appendiculatus which only spends 5 days on the host, at
each of its feeding stages, there is less acaricidal
pressure.
Agricultural
pesticides, including acaricides, have been
associated with several environmental and ecosystem damage. Different chemical
compounds have been used as acaricides, from organochlorines and arsenic to organophosphates and pyrethroids. One of the biggest impacts of cattle dips on
the environment is soil contamination. This usually arises from the disposal of
the waste liquid and sludge during dip tank emptying and refilling. Soil
contamination also occurs when there is leakage from the dip tanks as well as
at the chemical mixing areas should they spill (Livestock Production Program/Animal Health Program,
2003). The now more widely used pyrethroids have
been reported to have negative impacts on pasture fauna due to their
persistence in cattle dung (Vale and Grant,
2002). Mortalities and reduced reproduction of dung beetles and muscidae flies have been attributed to acaricide-treated
cattle in Australia (Wardhaugh,
et al., 1998) and Zimbabwe (Vale and Lovemore, 1999). Pyrethroids were detected in dung within days of
application and there was no loss in their concentration in the dung, two
months after use (Livestock
Production Program/Animal Health Program, 2003).
Breeding for tick
resistance
Sustainable control
of ticks and their resultant effects on livestock production can be achieved by
the selection of animals for increased resistance to ticks. This needs the use
of animals that transfer the genes to their offspring, consequently making a
population resistant. Anecdotal
evidence indicates that livestock breeds indigenous to an environment where
they are constantly challenged by disease or parasites have greater disease
resistance (Shyma et al. 2013). The purity of these
indigenous cattle breeds is now under threat due to breeding methods that
select against them in support of imported breeds. This natural resistance has
the potential to eventually reduce the need for the religious dipping of
cattle, leading to reduced cost of purchasing acaricides.
Crossbreeding has traditionally been used as a tick control method in many
countries with reports that it is effective, coming from some countries like
Australia (Sutherst, et al. 1979).
Genomic selection is
often the best way to improve traits that are hard to measure such as tick
resistance. The trait has often been avoided in many breeding programs because
it is very expensive, mainly due to the difficulty in locating the individual
animal variations. It is also laborious (Cardosso,
et al., 2021). Furthermore, previously there was no pressing need to
select animals for tick resistance (or disease resistance in general) as drug
therapy and prophylaxis were cheap, widespread and the unquestionable modus
operandi. However, the recent developments of increasing parasite
resistance to chemicals, economic challenges resulting in exorbitant costs of
drugs, and the new public preference for organically produced animal products,
especially those in the upper-end market, now make it more imperative that the
selection for tick resistance is taken seriously (Shyma
et al. 2013).
Previous studies have
reported low to high heritability for tick resistance depending on whether the
method used natural or artificial tick challenge, the size of the population
and the statistical method used (Regitano & Prayaga; 2010).
This has given hope for the use of this strategy in helping tick control
programs. The highly productive but disease and parasite-prone Bos taurus breeds
have been crossbred with the Bos indicus which have lower productivity but high
tolerance to ticks. These crossbreeding programs aim to have high production
while keeping tick infestation minimal. Therefore genetic evaluation of tick
resistance is important in gathering data and help to improve the tick
resistance trait in cattle (Mkize, et al.,
2021).
The
genetic control of animal host's resistance to ticks has always been known to
exist although it has been studied with a focus on the estimated breeding
values from the phenotypic data and little attention to the genes behind the
differences in the phenotypes (Goddard &
Hayes, 2009). The use of molecular biology techniques
and quantitative genetics has led to a better knowledge of the genetic
mechanisms behind the host's tick resistance being obtained. One such approach
is the use of genome-wide association studies (GWAS). This uses single
nucleotide polymorphisms (SNPs) to identify genetic variants of traits that are
complex (Mota et al., 2018). SNPs are
widely distributed in the genome and are heritable which makes them ideal in
studying and implementing genetic control strategies for improving tick
resistance in cattle through utilising markers associated with low tick load in
breeding schemes. GWAS tests each genetic marker independently for an
association with the trait while at the same time controlling for any possible
differences among animals caused by the breed (Neto, et al.
2010). Several quantitative trace loci (QTL) have been identified
using linkage analysis (Mapholi, et al., 2014).
However, successful application of this technique in developing countries is
still hurdled by the high costs of sequencing (Mkize et al, 2021).
Although
relatively few GWAS on tick resistance in cattle have been reported, especially
in Africa, there have been some interesting findings such as in Australia where
according to Barendse, 2007, several QTL
associated with tick infestation were identified in dairy cattle and beef
cattle of the Brahman breed (Patent No. WO2007051248-A1, 2007; Porto Neto et al., 2010; Turner et al., 2010). In
Brazil, a study on F2 of Gir cross Holstein cattle
identified QTLs associated with tick resistance on BTA 2,
10 and 23 during the dry season and BTA 5, 11, 23 and 27 during the wet season
(Otto et al. 2018). Various genes were identified that were associated with
tick count particularly TREM1, TREM2
which are important regulators of immune response and CD83 which is an
immunoglobulin superfamily protein. They used 23 microsatellite and 180
microsatellite markers ((Regitano & Prayaga, 2010; (Machado, et al., 2010). In
South Africa, Mapholi et al. (2016), in a GWAS on
tick resistance in Nguni cattle, identified several
genomic regions containing QTL for different tick count traits. They
identified three genome-wide significant regions on chromosomes 7 ( for total tick count on the head), 10 (for total body A. hebraeum tick count) and 19 (total A.
hebraeum on
the perineum region). A. hebraeum is an
important vector for heartwater disease in ruminants
in southern Africa. Some of these studies are summarised in table 1.
It is
to be noted that most of the GWA studies on cattle tick count data which have
been done to date rely on SNP chips for genotyping individuals which
particularly limits the discovery of novel markers as compared to other methods
such as whole genome resequencing (Korte and Farlow 2013; Pavan et al. 2020). Since
they only contain a subset of the SNPs, their low resolution typically may also
provide for more room to miss other genetic variants or markers that might be
of great significance.
An intergrated omic approach greatly
boosts the resolving power in narrowing down to QTLs that are of the most
significance in controlling specific phenotypes. In this regard, transcriptome studies are a valuable tool to support
evidence from other techniques as GWAS that exploit genomic polymorphism. A
study by Moré et al (2019) also showed the involvement of TREM2 a key gene involved in regulation
of immune responses as it was differentially expressed between the resistant
and susceptible cattle supporting the work done by Otto et al. (2018). They
also went on to identify other CD genes such as CD4 and CD14 that were coregulated in resistant hosts in response to tick
infestation. In addition, they also revealed that defensive responses such as
leukocyte chemotaxis and also skin degradation and
remodelling were amongst some of the mechanisms that conferred tick resistance
in Braford cattle.
Santos
et al. (2022), conducted a post-GWAS analysis using
the output from some of the studies mentioned earlier in combination with
sequencing data where they detected genes that showed possible structural
variants. They identified various genes that are involved in modulation of
eosinophil chemotaxis, monocyte differentiation and
also RIG-I signalling that included several genes that perform various immune
functions were also identified that included DAPK2, INPP5D, ACIN1 and PUM1. S. They also identified several transcriptional factor-gene networks
that are key in modulating responses to tick
infestation. These are shown in Figure 2.
In
addition to GWAS, genomic regions of interest can also be identified using regional
heritability mapping (RHM) (Nagamine et al., 2012; Riggio et al., 2013). RHM is a
variance component-based approach for mapping genomic regions influencing
complex traits, which combines information across contiguous SNPs. It is
a more robust tool that can pick those genomic regions containing multiple
alleles which each has little effect on variance such that they may not be
detected by GWAS. It also provides heritability estimates that are caused by
small genomic regions
The
advent of GWAS and RHM should lead to a new era in studies on host resistance
to ticks. Since there are many tick species affecting livestock in Africa,
future studies may focus on finding whether host resistance pathways are
similar or differ from one tick species to another. It can be safely argued
that there is great potential in the use of genomics to identify
genes responsible for tick resistance in cattle and in future provide a
complementary method for tick and tickborne disease
control for farmers (Penrith 2011).
CONCLUDING
PERSPECTIVE
The
impacts of ticks and the diseases they transmit have limited the development of
the livestock sector for a long time. Control of ticks has remained mainly
dependent on the use of acaricides. The modern era of
environmentally sustainable solutions to agricultural problems call for more
efforts to be placed on utilizing host resistance, and possibly anti-tick
vaccines to reduce the overreliance on acaricides.
New technologies in genomics offer hope for greater progress in the coming
years. True potential exists that genetic resistance can help solve the
environmental challenges created by use of chemicals. This will also add to the
economic benefits of reduced cost of purchasing the chemicals, improving the
productivity of and livelihoods in the semi-arid regions of the world that are
mostly affected by ticks.
Competing
interests: None
Author’s
contribution:
Stephen
Mandara: Conceptualisation, methodology, writing, review and editing.
Antony
Maodzeka: Methodology, writing, review and editing.
Acknowledgements:
Many thanks go
to our respective institutions for allowing us the material and time resources
to carry out this work.
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