COMMENTARY COMMENTARY When sex makes you sick

Marlene Zuk most important. A disease that spreads Department of Ecology, Evolution and Behavior, University of Minnesota, St. Paul, MN 55108 to both young and old can fluctuate wildly in the numbers of infected individuals in the population at any one time, with resulting Sex and parasites are two of the most important resulting in the evolution of elaborate orna- epidemics that sweep through an entire forces in evolution, shaping everything from ments that can only be produced by these population, leaving only resistant individuals theappearanceoforganisms(sex,byfavoring resistant males (5, 6). This kind of mate behind. The disease may then disappear, “ ” the evolution of ornaments and weapons) to choice can solve the lek paradox of loss of only to recur if infected visitors enter the their physiological functioning (parasites, via heritable in over con- population. In contrast, STIs can maintain selection for host defenses). They have been tinued selection because the genes in both more stable reservoirs with fewer large os- studied both separately and together, with host and parasite can cycle despite female cillations. This adult-to-adult transmission parasite–sex interactions similarly featuring preference for the same exaggerated trait. also means that STIs, unlike OIDs, give no in a wide range of areas in biology. Sexually Chronic parasites, such as helminths, rather opportunity for younger individuals, with “ ” transmitted infections (STIs) are, of course, than kill-or-recover infections, work best to their more malleable immune systems, to an obvious link between the two, but until favor such interactions. Note that such mate contract the disease and develop immunity now, little attention has been paid to the ways preferences for resistant mates are distinct after experiencing relatively milder symptoms, that both host and parasite can coevolve un- from those mate preferences in Ashby and asisthecaseformostso-called“childhood der this circumstance, and thus influence diseases”; instead, STIs encounter adult bodies both parasite virulence and host mating strat- The connection be- with full-blown virulence. They are rarely egies. In a set of models that incorporate the tween host life span immediately lethal, because they require their degree of mate choosiness as well as virulence and the outcome of host to be sexually active, which also means under different host life history states, Ashby that a range of virulences can be effective at and Boots (1) demonstrate how feedback be- host–parasite interac- maintaining the pathogen. At the same time, tween host and parasite can result in a variety tions noted by Ashby however, STIs in nonhumans are little studied, of outcomes for each party, from stable levels with most information available for domesti- of virulence and choice, to cycling between and Boots is particularly cated animals. high and low levels of each, to increasing interesting. Much work has been devoted to the ways that virulence of STIs can evolve to facilitate virulence, or to extinction. Their model also Boots’ model (1), in which individuals use transmission; for example, syphilis may have reveals the circumstances under which trans- mate choice to avoid becoming infected become more benign, with fewer obvious mission avoidance behavior, in the form of themselves. Third, selection for appropriate symptoms, just a few centuries after its in- choosiness for uninfected mates, is favored, host defenses in the context of life history troduction to Europe. Knell (10) suggests that and shows that such behavior is not univer- evolution can lead to sex differences in disease selection favored syphilis-infected hosts who sally favored by selection. susceptibility and longevity (7, 8). Among were able to continue having sex, and trans- The relationship between sex and parasites vertebrates, including humans, females are mitting the disease, something made easier if can take numerous forms, and it is useful to often more resistant to infections and also they were not covered in “Boils that stood out distinguish among them. First, parasites have live longer, traits that may be the result of like Acorns, from whence issued... filthy been implicated as a source of selection for differential selection on the sexes (7, 8). stinking Matter,” as was reportedly the case in models of the evolution of Last, some infections are primarily trans- in the 16th century. The syphilis bacterium sexual reproduction, with the advantage of mitted during sexual activity, the topic of may therefore have decreased in virulence generating new combinations of alleles off- Ashby and Boots’ paper (1). setting the cost of producing males (2, 3). as a response to selection for less apparent Under these scenarios, parasites with short What Makes Sexually-Transmitted carriers. Numerous studies have also ex- life spans relative to the life spans of their Diseases Special? plored whether secondary sexual characters hosts will be more likely to favor rapid cy- STIs are noteworthy, and distinct from what are honest indicators of resistance, with cling of host and pathogen genotypes. Several are sometimes called “ordinary infectious mixed results (6). The first type of effort fo- studies have found support for the predic- diseases” (OIDs), for several reasons (9). Al- cuses on the parasite, and the second focuses tions arising from this idea, with sexually though OIDs can be transmitted during on the host. Ashby and Boots (1) examine reproducing populations persisting longer sexual contact, STIs require it, which means both simultaneously, by tracing the effects of than asexual ones under pressure from para- transmission avoidance in mate choice on that STIs are more likely to be highly host- ’ sites (4). Second, because finding a mate with specific, setting the stage for the kind of tight both the host s choosiness and the virulence genes resistant to prevalent infections is al- coevolution in Ashby and Boots’ model (1). ways favored, regardless of the specific nature In addition, STIs, by definition, are mainly Author contributions: M.Z. wrote the paper. of the genes conferring such resistance, fe- transmitted between adults, influencing the The author declares no conflict of interest. males have been suggested to favor indicators rate of transmission and the life his- See companion article on page 13290. of disease resistance when choosing a mate, tory stage when defense against infection is 1Email: [email protected].

www.pnas.org/cgi/doi/10.1073/pnas.1518288112 PNAS | October 27, 2015 | vol. 112 | no. 43 | 13139–13140 Downloaded by guest on October 2, 2021 of the pathogen. Their model untangles long-lived, but both have a far shorter life some of Ashby and Boots’ predictions (1), a web of connections between choosiness, span than a sturgeon. Disease may be rela- including the relationship between trans- virulence, transmission rates, and disease tively rarer for the mayfly than the other two mission avoidance and virulence, but, more prevalence. species, as Ashby and Boots suggest (1), but broadly, it could lead to seeing how STIs and from the mayfly’s perspective, the distinction their influence on mate choice could, in turn, Longevity and the Price of Unsafe Sex is undetectable. How do the relationships affect other biological systems. For example, It is obvious that avoiding becoming infected ’ uncovered in Ashby and Boots models (1) Ashby and Boots (1) assume serial monog- duringsexisbeneficial,butatwhatcost? resolve themselves in nature? Related to this amy for simplicity’s sake, but how might Mate choice can be costly in terms of time issue is the question of the evolution of the avoiding infected partners lead to alterations spent searching, the cognitive or other ner- immune system itself; some authors have vous system ability to discriminate among in the mating system itself? When would suggested that insects and other inverte- selection for choosiness lead to the evolution potential partners, or the risk of predation brates lack an adaptive immune system of effective indicators of fitness, and when while traveling between mates (11). Previ- because their shorter life spans have meant would it favor cheating? What about the ously, the costs of mate choice have been that elaborate defenses against disease are “ ” operational sex ratio; does a decreased invoked in so-called good genes sexual not necessary (13). Again, however, lon- availability of one sex favor changes in selection, in which females prefer mates gevity is in the eye of the beholder, and the that bear genes conferring higher viability notion that insects are less likely to become virulence? Also, from the perspective of to their offspring, in contrast to a more infected is questionable, given the panoply the hapless individual that ends up mating arbitrary process in which male ornaments of diseases that specialize on invertebrates. with an infected partner, can any measures can become exaggerated simply through their The take-home message is that the role of counteract or ameliorate the risk of in- correlation with the preference for them demographic variables, including longev- fection? Self-medication has now been (11, 12). Arbitrary preferences can be ity, in the relationship between parasites described in a wide range of species, as maintained so long as the costs of choice and host mate choice remains open to have postcopulatory behaviors that may are minimal, but when being choosy carries exploration. serve to rid a recently mated individual of a price, indirect genetic benefits become Indeed, more research on STIs in a variety parasites (14, 15). Perhaps some of these more important. Ashby and Boots (1) take of organisms, including plants, is sorely characteristics can help make sex less of a this notion a step farther, showing that needed. Such research could be used to test risky business. when being choosy is costly, avoiding infected mates becomes prohibitively difficult, thus allowing the parasite to increase its virulence. 1 Ashby B, Boots M (2015) Coevolution of parasite virulence 8 Restif O, Amos W (2010) The evolution of sex-specific immune and host mating strategies. Proc Natl Acad Sci USA defences. Proc Biol Sci 277(1691):2247–2255. The connection between host life span and 112:13290–13295. 9 Lockhart AB, Thrall PH, Antonovics J (1996) Sexually transmitted the outcome of host–parasite interactions 2 Howard RS, Lively CM (2003) Opposites attract? Mate choice for diseases in animals: Ecological and evolutionary implications. Biol Rev noted by Ashby and Boots (1) is particularly parasite evasion and the evolutionary stability of sex. J Evol Biol 16(4): Camb Philos Soc 71(3):415–471. 681–689. 10 Knell RJ (2004) Syphilis in renaissance Europe: Rapid evolution of interesting. Cycling of host choosiness with 3 Ashby B, King KC (2015) Diversity and the maintenance of sex by an introduced sexually transmitted disease? Proc Biol Sci 271(Suppl parasite virulence is unlikely for short-lived parasites. J Evol Biol 28(3):511–520. 4):S174–S176. hosts, and those hosts with “intermediate” life 4 Lively CM (2010) A review of Red Queen models for the 11 Pomiankowski A (1987) The costs of choice in . persistence of obligate sexual reproduction. J Hered 101(Suppl 1): J Theor Biol 128(2):195–218. spans are most likely to be choosy, with be- S13–S20. 12 Andersson M (1984) Sexual Selection (Princeton Univ Press, nign parasites. Obviously, the model specifies 5 Hamilton WD, Zuk M (1982) Heritable true fitness and bright birds: Princeton). A role for parasites? Science 218(4570):384–387. 13 Vinkler M, Albrecht T (2011) Phylogeny, longevity and evolution the parameters for long vs. short life; however, 6 Balenger SL, Zuk M (2014) Testing the Hamilton-Zuk of adaptive immunity. Folia Zool Brno 60(3):277–282. in reality, organisms, whether host or patho- hypothesis: Past, present, and future. Integr Comp Biol 54(4): 14 Shurkin J (2014) News feature: Animals that self-medicate. Proc gen, cannot assess their own life span in either 601–613. Natl Acad Sci USA 111(49):17339–17341. 7 Zuk M, McKean KA (1996) Sex differences in parasite 15 Zuk M (2007) Riddled with Life: Friendly Worms, Ladybug an absolute or relative sense. Compared infections: Patterns and processes. Int J Parasitol 26(10): Sex and the Parasites That Make Us Who We Are (Harcourt, with a mayfly, a bumblebee is extraordinarily 1009–1023. New York).

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