Evolutionary Applications

In a recent Evolutionary Applications paper, Haig et al. (2016) presented an idea for the formation of a National Center for Small Population Biology. The paper was invited as part of a special issue dedicated to women in science (Wellenreuther and Otto 2016) where authors were asked to add a section to their papers that explored the idea of 'what would you do now in your career if you could do anything'. The Haig et al. paper focused on my scientific contributions; hence, the 'dream' section discussed a potential means to address my career-long interest in the science of small population conservation. Upon revisiting the paper in light of Smith et al., I found that an earlier version of the Haig et al. manuscript was inadvertently submitted and subsequently published by the journal, resulting in an unintended and inaccurate focus on the U.S. Fish and Wildlife Service (USFWS). The published paper was not vetted in accordance with the U.S. Geological Survey (USGS) policies meant to ensure the quality, utility, and integrity of USGS science. To meet these policies , USGS requires that information products, including journal articles, by USGS scientists receive review and approval at the highest level of the agency which confers the full weight of agency endorsement. Thus, the published version of Haig et al. does not represent the views of the USGS. I regret this error, particularly as USFWS is a close partner and we appreciate their scientific expertise. The 'dream' section was not intended to be specifically directed at the USFWS, nor did we attempt to identify the range of agencies and organizations that use specialized scientific information to conserve small populations. Rather, it focused on improving the scientific information available to all conservation groups and addressed the needs of wild species conservation in many parts of the world—similar to the work carried out for captive populations by the IUCN Conservation Breeding Specialist Group (CBSG: www.cbsg.org). Thus, it was meant to provide a broad overview rather than propose the specific details required for a National Center for Small Population Biology. Our vision was to optimize integration and application of existing expertise (including that of USFWS, USGS, and other agencies and institutions), regardless of where it would reside institutionally, as well as to expand capacities to meet specialized information needs for conserving small populations. The proposed Center would be multidisciplinary, drawing expertise from multiple fields (e. groups, …

Many parasites, including those of relevance to human health, use multiple hosts in order to complete their lifecycle. These complex lifecycles are somewhat mysterious from an evolutionary perspective, as the reliance on more than one host species seems likely to make the parasite more vulnerable to ecosystem perturbation and to restrict its range (L opez et al. 2015). There have been a number of intriguing hypotheses put forward to explain how selection could favor such strategiesranging from somewhat neutral explanations, such as selection to simply survive predation of hosts, to elaborately adaptive ones, such as selection to exploit hosts of larger size by moving up the food chain (Parker et al. 2015a;Poulin and Lagrue 2015). However, finding evidence to support these hypothesesand especially to craft generalizable explanationshas proved difficult.
One way to tease apart these hypotheses is to test the underlying assumptions of selection for expanded host use across systems. For example, what are the consequences of moving up the trophic ladder in terms of lost transmission opportunities or production of propagules? In their recent paper, Robert Poulin and Cl ement Lagrue aimed to quantify both asexual amplification in intermediate hosts and trophic transmission to definitive hosts for helminth parasites with complex life cycles (Poulin and Lagrue 2015). Looking across parasite species, the authors uncovered a positive correlation between asexual multiplication in the first intermediate host and parasite density at the next life stage for parasites with cercarial transmission (i.e. those with a free-swimming larval stage to move among hosts), but a drop in cohort density across stages for parasites with trophic transmission (i.e. those relying on predation of intermediate hosts). In both cases, however, the authors argue that the expansion occurring during asexual reproduction in the first host more than compensates for lost transmission later in the life cycle suggesting the costs of a complex life cycle might not be as large as expected.
Given the potential advantages of complex life cycles in terms of parasite amplification, the acquisition of host life stages might be predicted to be both adaptive and evolutionary labile. Recent work by Nate Hardy and colleagues utilized comparative phylogenetic analyses to explore the evolutionary flexibility of complex life cycles in aphids . By testing for correlations between life cycle complexity and plant host breadth or aphid reproductive mode, the authors discovered a positive relationship between heteroecy (lifecycle complexity) and polyphagy (the ability to eat a variety of food). They also found that life cycle complexity has evolved faster than the Aphidinae speciation rate, a result supporting the potential for rapid response of lifecycle complexity to selection.
The observed evolutionary flexibility of parasitic life cycles raises the possibility that parasites could adapt to multiple hosts simultaneously, using the same mechanism, without trade-offs between growth in one host and growth in another (however, see Parker et al. 2015b for cases where this might not be expected). Indeed, recent comparative work by Daniel Peterson and collaborators on host adaption in plant-feeding insects with pathogen-like life histories suggests that many adaptations allowing increased fitness on one host can also increase fitness on alternative hosts . Furthermore, the idea that having an obligate association with multiple host species necessarily limits a parasite's ability to jump to a new host or invade a new region has also been recently challenged. In their opinion piece, Miriama Malcicka and coauthors use the recent European invasion by the liver fluke, Fascioloides magna, a parasite with both an intermediate and final host, as a case study to emphasize the potential for rapid parasite range expansion and host jumps, even in the face of extreme ecophysiological requirements (Malcicka et al. 2015). If generally true, this would suggest parasites with complex life cycles should be more robust to changing abiotic and biotic conditions than might be expected based on their seeming specialization.
Overall, a better understanding of both the selection acting on parasites with complex life cycles and the consequences of these life cycles for adaptation, range expansion, and host switching is critical for predicting the emergence and spread of these often devastating parasites in human, agricultural, and natural populations (Buhnerkempe et al. 2015).

Britt Koskella Research Highlights Associate Editor
Evolutionary Applications