Tolerance: More Than Something Just Nice People Should Attempt

Many species change their distributions in response to climate change and anthropogenic translocation, increasing their likelihood of encountering non-native pathogens and herbivores.These species are often exposed to new pathogens and herbivores they have not adapted to, negatively affecting captive breeding and reintroduction programs. Based on ideas from theoretical research done host-parasite evolution, Jason Rohr and members of his lab (Matthew Venesky and Brittany Sears) from the University of South Florida, along with Peter Stiling (also from the University of South Florida) and Joseph Mendelson III (with the Department of Herpetology at the Atlanta Zoo)  recommend that selectively releasing tolerant  rather than resistant hosts maximizes the success of reintroduction and translocation programs in comparison to selecting for resistant hosts.

“The impetus for this study was the threat to biodiversity across the globe, in which infectious diseases have been an emerging factor,” says Matthew Venesky, first author of the paper and a postdoctoral researcher in Jason Rohr’s Lab. “In plant literature, two types of defenses to disease or parasites are studied: resistance and tolerance. In animal biology, however, tolerance has not been well studied. Neither has tolerance been studied in terms of conservation. It’s a fun idea.”

Selecting for resistance or tolerance invokes different selection pressures that impact the likely direction of evolution. While resistant hosts generally have a directly negative effect pathogens and herbivores, tolerant hosts generally have a neutral or sometimes positive effect on the pathogen and herbivore. In this way, resistant hosts promote the rapid evolution of increased virulence, compromising the viability of the host. The shorter generation time of most herbivores and pathogens in comparison to their hosts compounds the problem by allowing them to evolve increased virulence at a faster rate than their hosts can evolve a defense in response. Despite this seemingly obvious and clear-cut reasoning, many captive breeding and reintroduction studies focus on selecting for resistance or do not have an obvious aim to select one or the other. This study provides observational and logical proof that selecting for tolerance to a pathogen or herbivore will most likely lead to successful reintroduction of species under attack.

Two well-examined case studies establish support for host tolerance rather than host resistance: one on the pathogenic amphibian chytrid fungus (Batrachochytrium dendrobatidis, known as Bd) and the other on the herbivorous cactus moth (Cactoblastis cactorum).

Forty percent of amphibians are threatened with extinction, and infectious diseases such as Bd have been increasingly implicated. Because of the lack of a vaccine, the management of host populations via captive breeding has been the focus of most conservation efforts. Most studies that have focused on resistance, despite the fact that it can have negative long-term consequences: Bd evolves much faster than its hosts (four days versus three years), making it likely that introductory resistance could lead to an increase in virulence. In addition, conducting studies that select for resistance require a proportion of frogs in each clutch to die, whereas studies selecting for tolerance do not have to. A possible way to select for tolerance is to identify traits of amphibians that could reliably predict tolerance to Bd without pathogen exposure. Unfortunately, data regarding the immune mechanisms that provide resistance to Bd is scarce. The fact that some amphibian species appear to be tolerant of Bd—indicating that there may be some unidentified tolerance mechanism—is encouraging.

The cactus moth is native to eastern South America and has been used around the world to control non-native prickly pear, which has colonized a lot of land and made livestock grazing impossible. The cactus moth was introduced to the Lesser Antilles but it spread to the Greater and Antilles and from there colonized the US. It is predicted to inhabit much of Mexico and the Southwestern US. The cactus moth threatens two rare cacti (the jumping cactus and the semaphore cactus) endemic to the Florida Keys that exist in populations of 15-100 adults on just 1-2 islands. In 1990, botanists collected juvenile individuals of adult semaphore cacti and propagated them without artificially selecting any traits. Some cacti were replanted a decade later but were colonized by the cactus moth, and only 3.3% remain alive. Data suggests, however, that some individuals of prickly pear are tolerant of herbivory. In South Africa, prickly pear with tolerance to cactus moths rapidly abscised stressed pads (e.g. those colonized by cactus moth larvae), thus increasing their rate of reproduction because prickly pear reproduction involves growth from fallen pads).

A cactus affected by cactus moth herbivory.
From: http://www.desertmuseum.org/invaders/invaders_cactusmoth.php

“One criticism we anticipate that we discussed in the paper is that selecting for tolerance in a host could lead to flourishing populations of the parasite or herbivore. The overall increase in pathogen or herbivore abundance could facilitate the spread of the species beyond the area already occupied by the tolerant host, furthering the need to select more species or populations for tolerance.” says Venesky. Another potential negative consequence is that the increase in tolerance may result in tradeoffs with other important traits, thus compromising long-term population viability.

In conservation biology, a persistent issue is prioritizing efforts. In captive breeding and the consequent reintroduction programs, the most efficient method would likely be to select for tolerance in species that are experience rapid population decline or are already in danger. “You really have to weigh the costs and the benefits,” says Venesky. “We really have our hands cuffed with amphibian loss occurring at such a high rate, and we really need innovative approaches.” These case studies are encouraging because they not only provide exemplary success stories in favor of tolerance selection, but provide conservation biologists with a clear, fairly non-invasive and non-radical “recipe” to follow.

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