Parasites and other pathogens are generally smaller than their hosts are and reproduce faster. Consequently, one might expect them to win any arms race because, potentially, they could evolve adaptations to overcome their host’s defences faster than the host could generate new ones. However, hosts that are comparatively long‐lived usually have sophisticated immune systems that identify and kill or neutralize new parasite variants. The host is therefore not a constant environment for the parasite. Parasite virulence is also affected by the mode of transmission. Horizontally transmitted parasites, especially those with a wide host range, can ‘afford’ to be highly virulent because there are lots of potential hosts and if one or more of them dies it has no direct consequences. However, when the parasite is vertically transmitted (e.g., via the eggs of its host or across the placenta) there is a direct link between the effect of the parasite on its host and its own reproductive success. For example, a virulent parasite’s genes will not be transmitted; if the parasite is so pathogenic, it kills the host before it can reproduce. Similarly, if it kills the host’s eggs while they are in utero or reduces the number of host eggs that are produced or survive to become adults and reproduce themselves, then the parasite is compromising its own reproduction. It is therefore to be expected that, as a rule (there will always be exceptions), vertically transmitted parasites should be less pathogenic than those that are transmitted horizontally. There is some support for this hypothesis. For example, two ectoparasites of swifts – a louse and fly – that are vertically transmitted have no effect on nestling growth or fledgling success even when the numbers of these parasites are artificially increased or the birds are stressed (Tompkins et al. 1996). Similarly, in feral pigeons, a vertically transmitted louse has little impact on the birds’ health but horizontally transmitted ectoparasitic mites cause so much distress that the birds’ reproductive success drops to zero (Clayton and Tompkins 1995).
1.5.2 Parasites in the Fossil Record
Most parasites are soft‐bodied organisms, and they lack the hard structural features that facilitate preservation in the fossil record. It is therefore impossible to ascertain whether parasitism has always been a common ‘lifestyle’ – although this is highly likely. Conway Morris (1981) suggested surveying the commensals, symbionts and parasites of those organisms that have remained apparently unchanged for millions of years (the so‐called living fossils) might reveal unusual organisms and provide insights into animal associations. For example, horseshoe crabs (Phylum Chelicerata, Subclass Merostomata) have existed almost unchanged for hundreds of millions of years. There is little published information on their parasites although flatworms of the family Bdellouridae only form associations with them (Riesgo et al. 2017). Despite the paucity of the fossil record, studies to date suggest that many parasite–host relationships persist for millions of years, and that parasite life cycles and morphology remain remarkably constant (Leung 2017)
Copepod ectoparasites that were morphologically similar to those in existence today have been identified attached to fossil teleost fish dating to the Lower Cretaceous Period (145–100.5 million years ago) (Cressey and Boxshall 1989). Evidence of nematode parasites is largely restricted to those infecting insects that became trapped in amber (Poinar 1984). Helminth eggs can be identified in coprolites (fossilised faeces), but while there have been extensive studies on animal and human faeces found in archaeological sites (Camacho et al. 2018), there is less data on coprolites dating back millions of years. As with any faecal analysis, one must not assume that presence indicates parasitism. An organism’s presence may result from passage through the gut following accidental consumption (e.g., eggs of a parasite of another animal) or invasion of faeces after its deposition (e.g., eggs of a detritivore). Preservation of animals following rapid mummification under desiccating conditions or freezing in tundra enables the identification of soft‐bodied parasites with greater accuracy. For example, nematodes and botfly larvae can be identified from woolly mammoths that died thousands of years ago on the Siberian tundra (Grunin 1973; Kosintsev et al. 2010).
Sometimes one can infer the presence of parasites in fossilised remains from the pathology they cause (Donovan 2015). For example, the pearls found in mussels and oysters often form because of infection by trematode parasites. Pearls thought have been caused by trematode parasites have been identified in fossil mussels dating back to the Triassic era (250–200 million years ago) (Newton 1908). Dinosaurs almost certainly had their full complement of parasites although their evidence is sadly lacking from the fossil record. However, marks found on the bones of the dinosaur Tyrannosaurus rex are thought to resemble the pathology caused by the protozoan parasite of birds Trichomonas gallinae (Wolff et al. 2009). Similarly, Tweet et al. (2016) found sufficient evidence in the fossilised gut contents of a hadrosaurid dinosaur to describe a vermiform organism that they called Parvitubilites striatus that may have been parasitic. Poinar and Poinar (2008) have even suggested that parasites were a major factor in the ultimate extinction of the dinosaurs – although this is not a widely accepted view amongst palaeontologists.
1.5.3 Parasites and the Evolution of Sexual Reproduction
Sex has fascinated biologists (amongst others) for generations. From a logical point of view, sexual reproduction does not make sense because of what is referred to as the two‐fold cost of sex. Firstly, the males, who usually constitute in the region of 50% of a population, serve only to inseminate the females and do not reproduce themselves. Furthermore, a lot of time and effort is often employed in searching for a mate and mating can itself be an energetically expensive and potentially dangerous process. By contrast, in an asexually reproducing organism 100% of the population can reproduce. Consequently, an asexually reproducing population is theoretically able to grow faster and respond to changes in the environment (e.g., increased food supply) faster than one that reproduces sexually. The other ‘cost’ of sexual reproduction is that the gametes are haploid and the process of recombination at meiosis means that an individual can only pass on 50% of its genes to each of its offspring. Consequently, useful genes and gene combinations could be lost in the process of generating new genetic variants. Despite these problems, and several others, most organisms undertake sexual reproduction and therefore it must have some major advantage(s)
There are several theories why so many organisms reproduce sexually (Burke and Bonduriansky 2017). One of the most popular is that of Hamilton et al. (1990) who suggest that sexual reproduction arose as a mechanism by which organisms can limit the problems of parasitic infections. Parasites can potentially reproduce faster than their hosts, and therefore, they will evolve to overcome the most common combination of host resistance alleles. Therefore, hosts with rarer resistance alleles will then be at a competitive advantage and ultimately one of these will become the most common resistance allele combination in the host population. The arms race will continue ad infinitum with the parasites adapting to the most common resistance allele combination and the host generating new allele combinations. The process of recombination ensures that (provided the initial gene pool is sufficiently diverse) there will be a constant supply of novel resistance alleles. Furthermore, a resistance allele combination to which parasites have adapted need not be lost from the population because it may prove useful again in the future. By contrast, in an asexually reproducing organism the offspring will have the same resistance allele combinations as their parents, and once parasites have overcome these, then the whole population is vulnerable to infection.
If sexual reproduction arose as means