As our social media feeds flood with predictions of global devastation at the hands of human induced climate change it becomes increasingly important in the world of biology to accurately model the consequences of environmental upheaval for species and ecosystems. On Friday 15^th March 2019, 1.4 million people took to the streets of cities across the world to persuade governments to act to reduce carbon emissions by 40% within the next 12 years and prevent irreparable damage to our planet. Climate change is one of the most talked about subjects of the 21^st century, and rightly so. Whilst conservation efforts intensify by the year, the focus is on large free- living species, leaving parasitologists calling for increased efforts to protect all of the worlds fauna. As we consider the future of our world, it is important to remember that climate change will affect every species, even the smallest amongst us. I’m talking, of course, about parasites. So, what does climate change mean for parasites?

Despite global efforts to conserve our unique and diverse biota, parasite conservation remains, at least in my opinion, largely overlooked. It is only at the end of the 21^st century where researchers began to turn their attention to the effects of climate change on parasites. The most comprehensive description of the challenges of climate change for parasitic species was published by Carlson et al., (2017), who report that under conservative, best case scenarios of climate change, 5 to 10% of parasite species face extinction by 2070 as a result of climate- driven habitat loss. When the researchers incorporated the predicted loss of host species, this figure rose to 30%. However, the parasite species that can tolerate these new conditions will be able to invade new ecosystems, replacing native species. Both the extinction and the replacement of a parasitic species can have unpredictable consequences for the host species, and the ecosystem it inhabits.

Parasites are not only threatened by climate change and loss of habitat in free- living stages, but face threats unfamiliar to free- living species. Parasitism is a life strategy that requires a host; in this way parasitic species are dependent on the survival of their hosts. Additionally, host population density must be above a certain threshold for the transmission, and therefore survival, of the parasite. However, as contradictory as it seems, conservation efforts to protect hosts might further diminish the survival of their parasites. Veterinary treatment to reduce disease transmission in managed animals is common in conservation strategies such as reintroduction, translocation and captive management. These methods result in the loss of many of the natural enemies of species, including parasites.

But aren’t parasites pests? Why should we worry about parasite extinction? The loss of parasites might be good news for their free-living hosts, but could have large, unpredictable consequences for everything else. As Gómez and Nichols (2013) so adeptly put it, the ‘arguments for the conservation of any species apply equally well to parasites.’ Parasites are estimated to comprise ½ of all species and no species is exempt from parasitism; they are the most common and influential life form. In this way parasites provide a large factor in host biology and evolution. Parasites have a large role in individual fitness, species evolution and ecosystem organisation. Parasitism inevitably involves a fitness cost to the host, which reduces the amount of energy to expend into reproduction, even in the absence of disease. Furthermore, in some cases, parasitism can result in the death of the host. In this way, parasites provide top-down control of host populations, and are a vital component of all ecosystems. Whilst this on its own is good cause to protect parasites, the effect of parasitism on hosts provides a selection pressure, which can impact the evolution and niche of hosts. Besides, parasitic infection isn’t always doom and gloom. As Gómez and Nichols (2013) argue, some parasites provide cross- immunity for infection with other species of parasites and some have been cited to remove harmful substances from their hosts.

And if I haven’t convinced you about the value of parasite conservation, parasites can give researchers a lot of information about ecosystems and can be useful in the study of the evolutionary history of organisms. The presence and composition of parasitic species has been a useful indicator in the assessment of the health of populations and ecosystems. A diverse range of parasitic species indicates that the system has been less impacted by human activity. In this way, parasites themselves might be crucial in current conservation efforts for other species and ecosystems.  Excluding parasites from conservation efforts in this period of dramatic climate change will mean that we will lose species that form a critical component of biological processes.

Now, if I’ve convinced you, the question is how to go about conserving parasites. Whilst most conservation efforts and literature focus on free- living species, the same principals can be applied to the conservation of parasites. This is not to say that parasite conservation is straightforward; the conservation of parasites will require a drastic public relations makeover; the conservation of parasites will preserve many of the pathogens of wildlife, domestic animals and humans. Furthermore, there are a litany of issues surrounding the classification of many parasite species and clades.  A large portion of parasitic species remain undescribed, and as such might not be understood or protected in time. There is still a large amount of work to be completed before we fully understand the world of parasites, and we can give our all to their conservation.

Whilst parasites might not be the prettiest, most likable or most friendly of creatures they still require the same consideration that we give to other species; as Gómez and Nichols eloquently write ‘notions of intrinsic value are applicable regardless of trophic strategy, and there is no reason why beauty cannot be found in parasite morphology, behaviour, or natural history.’ On that note, I’ll leave you to ponder the problem of pest protection.

Sources:
Carlson et al., 2017
access here.

Gómez and Nichols, 2013
access here.

Parasites are ubiquitous; they are found on every continent, in every country and every in population of animals. Parasitism is an inescapable component in the evolution of species, and can affect the development, behaviour and reproductive success of individuals. However, parasites are almost never distributed evenly amongst individuals and populations. Individuals and populations frequently have varying degrees of parasite burdens. The uneven distribution of parasites leads to variation in the intensity of selection, which can then shape patterns of disease occurrence, host evolution and host- parasite interactions.

In the immortal words of Terry Pratchet “If you do not know where you come from, then you don’t know where you are, and if you don’t know where you are, then you don’t know where you’re going. And if you don’t know where you’re going, you’re probably going wrong.”. To phrase it differently, to understand host-parasite interactions and their consequences, you need to first understand the evolutionary history and biological underpinnings of parasitic tolerance in individuals and populations.

So, a big question in parasite ecology is what does this uneven distribution mean for hosts? To answer this, you first must begin with asking the question ‘where does this distribution come from originally?’ It is this question I have chosen to answer in my dissertation.

When I first began to scour the literature, it became clear that evolutionary trade-offs play a large role in resistance, or lack thereof, to parasites. Biologists have long proposed evolutionary compromises, or trade- offs, in the investment of energy by individuals into traits that have a clear impact on reproductive output, known as life history traits. Think of it this way, an individual has access to a finite amount of resources, and so has a finite amount of energy to expend into life history traits, such as immunity and reproduction; individuals invest energy into one trait at the expense of investment into the other.

In the world of parasite ecology, researchers have repeatedly found evidence of a trade- off between immune function and hormone production which correlates with parasitic resistance. In this hypothesis, high levels of circulating hormones have been shown to supress the immune function of individuals. At first this sounds like a no brainer, surely it is more practical for an individual to invest everything into immunity to defend against disease. Nevertheless, hormones, such as testosterone, provide individuals with a reproductive advantage, and individuals must strike a balance in investment. Males with high levels of testosterone are likely to be more aggressive and so better able to defend territories as well as having improved sperm competition.

Research has shown that, yes, increased investment into hormone production is correlated with lowered investment into immune function and higher parasitic burdens in a number of rodent species. For example, Barnard et al., (2002) show that isolated populations of voles with high levels of parasitic infections, males have larger adrenal glands, testes and seminal vesicles for their age and weight. These organs are involved with the production of hormones and are correlated with higher levels of androgen function. Furthermore, female voles with high parasite burdens also had larger adrenal glands. This suggests that there has been an evolutionary pressure from sexual selection for increased androgen levels, which has suppressed the immune system resulting in high infection intensities. Additionally, in spiny mice a composite measure of androgen function, which includes aggressive behaviour, circulating hormone levels and organ weight associated with androgen function showed a positive relationship with parasite burdens.

Barnard et al., (2003) conducted an interesting experiment to measure the effect of an individual’s environment on behaviour. By interesting, I mean they conducted social discrimination tests of aggression between male spiny mice from different populations with varying parasitic intensities. This study showed that individuals taken from populations with a higher infection level showed a lower level of aggression towards novel mice. As I mentioned before, high levels of androgens can result in aggressive behaviours, but in this case populations with high parasitic infection levels, and high levels of circulating androgens, individuals were less aggressive in order to reduce the risk of infection. This is evidence that individuals regulate their behaviour based on the perceived risk infection, rather than their individual burden or level of androgen production.

In terms of evolutionary pressure to invest into immunity, Ponlet et al., (2011) demonstrates that female rodent species with high diversities of gut parasites have larger spleen weights on average. The spleen is involved in the production of lymphocytes, and an integral component of resistance to parasitic infections. This shows that parasites provide a selective pressure to increase investment into immunity. On the other hand, Ponlet et al., (2011) also shows that male rodents exhibit a plastic response to parasitic infection, were individuals with higher burdens had larger spleens, regardless of the average infection level in the species.

There is likely a complex relationship between hormone function, immunocompetence and parasitic infections, which is why for my dissertation, I have decided to take the leap to identify a trade-off between hormone function and immunocompetence in order to explain the current distribution of gut parasites. I have also decided to analyse the differences in this trade-off between populations to find evidence of an evolutionary response to selective pressures. To complete this I have analysed anatomical and morphometric data from four semi-isolate populations of spiny mice (Acomys dimidiatus). As well as being incredibly cute, the spiny mouse is the numerically dominant rodent in the South Sinai region of Egypt, an area that is undergoing dramatic climatic change and a decade long drought. 91% of the specimens collected were infected with at least one species of parasitic gut helminth, and the structure and abundance of these helminth communities were found to vary between populations, and over time. With any luck, I’ll be back in 2 months time to tell you why!

Sources:
Barnard et al., 2002.
access here.

Barnard et al., 2003
access here.

Ponlet et al., 2011
access here.

If you happen to own a cat, I’m sure you’re well versed in the ordeal of coaxing your companion to the dreaded vet to be poked, prodded and medicated to eradicate their pesky fleas. Despite the trauma, when the prodding is over and done with, and the pest has been exterminated, your beloved pet will thank you. Pet owners all over the world know the struggle; they face the same common enemy- the common cat flea, Ctenocephalides felis. This particular pet pest presents parasite ecologists a near unparalleled success story of world domination.

Not only is the flea a threat to the comfort of pets everywhere, they can transmit bacteria to humans, including the bubonic plague, cat scratch fever and typhus. As we urbanise our towns and cities, building roads wherever we might go, contact between wild and domestic animals becomes increasingly common. In this way, fleas carrying disease can find their way to humans, resulting in outbreaks of disease. For this reason, it is important to understand the biology of the common flea species to better control outbreaks of disease.

A publication by Lawrence et al., (2019) from the University of Sydney shows that 93.1% of fleas collected from domestic animals worldwide are from the genus Ctenocephalides. However, until the publishing of this study, the phylogeny and genetic identity of the genus remained poorly understood. The study describes the most comprehensive model of the evolution of the most common species and subspecies of Ctenocephalides and addresses the question of what made the flea so successful in a wide range of climates.

The study began with the collection of the most common Ctenocephalides species and subspecies from a number of countries across the globe. These specimens were then genetically analysed and taxonomically identified using morphological characteristics. The sequence data gathered was used to determine the evolutionary relationships between the lineages through a multigene alignment of 2 mitochondrial genetic markers and 2 nuclear genetic markers. This data was further used in combination with morphological data to find the genetic identity of species, to determine whether or not species and subspecies had any distinct genetic markers that are not shared with other lineages. This data was also used to estimate the likelihood of the most recent common ancestor of the genus originating from each continent, the age of each lineage, and the diversity of each community.

Previous research classified the most common fly species found on domesticated animals as 4 different Ctenocephalides species: C. canis, C. orientis, C. damarensis and C. felis. These had been characterised as species by their morphology and host preference, and their genetic identity remained poorly resolved. Furthermore, C. felis was particularly taxonomically ambiguous, with a number of morphologically distinct subspecies, Ctenocephalides felis felis, C. f. strongylus, C. f. ‘AL909’ and C. f. ‘transitional’. Whilst this species comprised 85% of all fleas collected from domesticated animals across the globe, the taxonomy of the subspecies was not understood, nor had research been carried out to determine the genetic identity of the lineages.

The phylogenetic produced grouped all the subspecies of C. felis with C. damarensis, suggesting that C. damarensis is a subspecies of C. felis. Additionally, genetic sequences of C. damarensis were never grouped together in genetic analysis, suggesting that the lineage is in fact a subspecies, and had been wrongly classified as a species in the 1990s. C. canis and C. orientis were confirmed as a monphylectic group, which is unsurprising given their shared affinity for canine hosts.

This paper is a good example of the taxonomic crisis rattling parasite ecologists today. Parasite species are thought to comprise ½ of all species on Earth, yet the vast majority remain undescribed. This paper shows that research using morphological characteristics to identify species is more likely to result in the false classification of a species than genetic techniques.

The genetic sequences taken from C. felis were never clustered by their presumed subspecies identity; Lawrence et al., identified 8 clades of C. felis in their analysis, which can be grouped into 4 climactic clusters dependant on the environmental conditions required for the maximum growth and reproduction of the lineages.

The oldest communities of Ctenocephalides were found in Africa, as African communities showed the highest genetic diversity. The continent also had the highest likelihood as being the origin of the genus. Furthermore, all 8 clades of C. felis were found there, suggesting that Africa is the evolutionary cradle of the common cat flea. However, within C. felis, some clades showed evidence of a more recently European ancestral line. C. canis and C. orientis show recent European and Asian ancestry, which correspond with dog domestication events in these locations.

The study proposes that the cat flea evolved alongside the African wildcat, the ancestor of the domestic cat, which ranged from Africa into the near East. From there, lineages spread throughout the world; the next oldest C. felis flea communities were found in Asia and Europe, then Oceania and lastly the Americas. The establishment of these communities across the globe corresponds with cat domestication events and human mediated translocation of cats. Only the temperate clades of C. felis were found on every continent; the success of the temperate lineages of C. felis begs the question; why is this lineage so successful?

The temperate lineages of C. felis demonstrate an uncanny ability to survive in a wide range of ecological conditions. Ectoparasites with ‘off- host’ life stages are dependent on specific environmental conditions, such as temperature and humidity, for the maximum rate of growth and reproduction. The researchers modelled environmental conditions and species distribution to identify which factors are the most significant in predicting distribution. Conditions associated with cooler climates were found to be the largest predictor of the distribution of temperate lineages, and these lineages were found to be able to tolerate a wider range of climates, and be more successful than their temperate and African counterparts at lower tempersatures.

European maritime exploration from the 15^th-19^th century took cats and dogs all around the world. The tolerant temperate fleas hitchhiked on these expeditions on the backs of hosts. I mean, who doesn’t want to travel? This allowed the temperate clade 1 of C. felis to be introduced to all continents and to interbreed with existing populations, making it the world’s premier pet pest that we recognise today.

So next time you wrestle your cat into a carry case, give a thought to the long and unique story of the common cat flea. The Ctenocephalide fleas have achieved world domination by hitchhiking human travel, making their way from continent to continent, invading population after population of unsuspecting hosts. The uncanny ability of these species to tolerate a broad spectrum of environmental conditions makes them the perfect candidate to seize any opportunity to spread to novel environments.

Source: Lawrence et al., 2019.
access here.