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Jenna M. Hulke and Charles D. Criscione: Read the article
Hulke and Criscione found that high selfing rates for a trematode could be explained solely by demography. Using demographic estimates of selfing, they found no evidence for inbreeding depression. Their study tests a theory for why parasites maintain complex life cycles.
Why are complex life cycles found throughout nature, and how do they arise?
Some familiar examples include crawling caterpillars metamorphosing into airborne butterflies or aquatic tadpoles transforming into land-dwelling toads. Perhaps lesser-known examples are parasites who require multiple hosts, ranging from small invertebrates (snails, molluscs) to larger vertebrates (fish, birds) to complete their life cycles. One specific group of these is Trematoda: parasitic flatworms. Trematodes typically reproduce sexually in a predator host (“definitive” host), who then excretes the parasite’s eggs. These are often consumed by one or more prey hosts (“intermediate” host), where the parasite asexually reproduces. The cycle repeats when the definitive host eats the intermediate host.
How can this particularly complex life cycle be beneficial? Why use multiple hosts when there are so many potential risks along the way, such as transmission failure? A few theories have been put forth in the literature. In 2001, S. P. Brown and colleagues proposed that having multiple hosts and only sexually reproducing in the final host may help parasites avoid reduced fitness in the form of inbreeding depression. Why? Parasite abundance is amplified with each successive transmission up the trophic pyramid. Therefore, there are more available mates in the predator host, reducing the chances of inbreeding. This evolutionary pressure would maintain the complex life cycle of having multiple hosts.
In their article “Testing the mating system model of parasite complex life cycle evolution reveals demographically driven mixed mating,” Hulke and Criscione aimed to empirically test Brown et al.’s theories, something that has been rarely done, by quantifying inbreeding and inbreeding depression in samples of the hermaphroditic trematode Alloglossidium renale. Phylogenetic evidence suggests that A. renale lost its third host, leading to a “truncated” life cycle. This left only the first two intermediate hosts – snail and shrimp – in which to reproduce asexually and sexually, respectively. Hulke and Criscione therefore posited that if Brown et al.’s theories were correct, they would observe the presence of inbreeding but the absence of inbreeding depression in the second host, which would have allowed the third host to be lost over evolutionary time.
The authors collected four sample sets of A. renale (sexually mature individuals living in their second shrimp host) across small bodies of water in Louisiana, Mississippi, and Texas. The authors sequenced their DNA and calculated the genetic selfing rate (sG: the number of individuals produced via selfing) and accounted for false signatures. They then calculated the demographic selfing rate (sD), or the expected “null” rate of selfing, given a randomly mating population. Uniquely, sD was derived from the average infection intensity, or the number of parasites in the focal gland. sG < sD would indicate that fewer genetically inbred individuals were surviving to adulthood, equating to inbreeding depression.
The authors found that sG estimates were both very high and very similar across all sample sets, i.e., all sets had high levels of inbreeding. Additionally, they found no significant differences between sG and sD, i.e., there was no evidence of inbreeding depression across all sets. These findings were in line with Brown et al.’s ideas. A. renale having high levels of inbreeding but no evidence of inbreeding depression lent support to the theory that inbreeding depression avoidance in other multi-host systems could maintain the three-host complex life cycle.
In this article, Hulke and Criscione presented a new method for measuring inbreeding depression in parasite samples collected from the field, removing the necessity of maintaining difficult lab populations and thereby facilitating more studies. Additionally, many theories for the evolution of mixed mating systems invoke selection. However, the authors assert that because their genetic selfing rate matched the “null” demographic expectation, demography is the primary (and perhaps singular) driver of A. renale’s mating system, not natural selection. This study offers an exciting foundation for future studies in evolutionary parasitology. It also challenges us to rethink our assumptions around the relative roles of selection, demography, and random chance in shaping the evolutionary trajectories of the organisms around us.
Faye Romero is a PhD candidate and NSF GRFP Fellow at the University of Rochester in Dr. Nancy Chen’s lab. She is investigating the underlying genetic causes of inbreeding depression in the Federally Threatened Florida Scrub-Jay. Faye is also an avid swing dancer and birdwatcher, and is passionate about increasing accessibility to STEM careers for young people.