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 of reducing the depredations of parasites, then one would expect it to be common where parasites are abundant and challenge frequent. By contrast, asexual reproduction should be favoured where parasites are absent, or the level of challenge is low. Although there are several instances of exactly this in the literature, they remain remarkably few. The best‐known example is that of the snail Potamopyrgus antipodarum that originated in New Zealand and has since spread to many parts of the world. It exists as sexually reproducing populations, asexually reproducing populations, and mixed sexually and asexually reproducing populations. Positive correlations have been described between the extent of parasitism by parasitic flatworms and the frequency of sexual reproduction. Sexual reproduction is rare where flatworm parasite challenge is low, and conversely, it is common where the parasite challenge is high (Lively and Jokela 2002). Another commonly cited example is that of certain minnow populations living in Mexico (Lively 1996). These minnows exist as both asexually reproducing and sexually reproducing populations, but those reproducing sexually tend to have lower parasite burdens (except where inbreeding has resulted in reduced genetic diversity). Most multicellular parasites reproduce sexually themselves, although some combine it with asexually reproducing larval stages, such as schistosomes and the tapeworm Echinococcus granulosus. Even some parasitic protozoa, such as the trypanosomes, exhibit something akin to sexual reproduction. This suggests that even endoparasites living in protected environments such as the gut or bloodstream of another animal remain vulnerable to infections. However, although there is experimental evidence that parasitism influences the evolution and maintenance of sexual reproduction (Auld et al. 2016), there are almost certainly many other factors involved. For example, sexual reproduction may help protect against transmissible cancer cells (Thomas et al. 2019).
1.6 Parasitism as a ‘Lifestyle’: Advantages and Limitations
Provided one can get away with it, stealing something is easier than making it oneself or earning money to purchase it. Therefore, it is unsurprising that so many organisms have adopted a parasitic lifestyle to some extent. If one takes the view that the main purpose of an organism’s existence is to transfer as many of its genes as possible into the next generation, then all organisms should maximise their reproductive output. However, an organism must trade the costs of reproduction against other activities such as finding food and then digesting and absorbing it, finding a mate, and protecting itself against competitors, predators, and the environment. By living upon or within a host, a parasite can reduce many of these ‘other costs’ and thereby devote
