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Parasitic worms (i.e., helminths) commonly infect multiple hosts in succession. With every transmission step, they risk not infecting the next host and thus dying before reproducing. Given this risk, what are the benefits of complex life cycles? Using a dataset for 973 species of trophically transmitted acanthocephalans, cestodes, and nematodes, we tested whether hosts at the start of a life cycle increase transmission and whether hosts at the end of a life cycle enable growth to larger, more fecund sizes. Helminths with longer life cycles, that is, more successive hosts, infected conspicuously smaller first hosts, slightly larger final hosts, and exploited trophic links with lower predator–prey mass ratios. Smaller first hosts likely facilitate transmission because of their higher abundance and because parasite propagules were the size of their normal food. Bigger definitive hosts likely increase fecundity because parasites grew larger in big hosts, particularly endotherms. Helminths with long life cycles attained larger adult sizes through later maturation, not faster growth. Our results indicate that complex helminth life cycles are ubiquitous because growth and reproduction are highest in large, endothermic hosts that are typically only accessible via small intermediate hosts, that is, the best hosts for growth and transmission are not the same.

Classical theory on mating system evolution suggests that simultaneous hermaphrodites should either outcross if they have high inbreeding depression (ID) or self-fertilize if they have low ID. However, a mixture of selfing and outcrossing persists in many species. Previous studies with the tapeworm Schistocephalus solidus have found worms to self-fertilize some of their eggs despite ID. The probability for selfing to spread depends on the relative fitness of selfers, as well as the genetic basis for ID and whether it can be effectively purged. We bred S. solidus through two consecutive generations of selfing and recorded several fitness correlates over the whole life cycle. After one round of selfing, ID was pronounced, particularly in early-life traits, and the conservatively estimated lifetime fitness of selfed progeny was only 9% that of the outcrossed controls. After a second generation of selfing, ID remained high but was significantly reduced in several traits, which is consistent with the purging of deleterious recessive alleles (the estimated load of lethal equivalents dropped by 48%). Severe ID, even if it can be rapidly purged, likely prevents transitions toward pure selfing in this parasite, although we also cannot exclude the possibility that low-level selfing has undetected benefits.

Switching from one host to the next is a critical life-history transition in parasites with complex life cycles. Growth and mortality rates are thought to influence the optimal time and size at transmission, but these rates are difficult to measure in parasites. The parasite life cycle, in particular the trophic link along which transmission occurs, may be a reasonable proxy for these rates, leading to the hypothesis that life cycle should shape life-history strategy. We compiled data on the size and age at infectivity for trophically transmitted helminths (i.e., acanthocephalans, cestodes, and nematodes), and then categorized species into trophic links (e.g., planktonic crustaceans to fish, insects to terrestrial vertebrates, etc.). Comparative analyses that explicitly included stabilizing selection within trophic links fit the data significantly better than random walk models, indicating that parasites with different life cycles have different optimal times/sizes for host switching. The major helminth groups have often independently evolved similar life cycles, and we show that this has frequently led to convergent and/or parallel evolution of size and age at infectivity. This suggests that for particular life cycles there are universal optimal transmission strategies, applicable to widely divergent taxa, although the cases of parallelism might indicate that lineage-specific constraints sometimes prevent evolution to a single adaptive peak.