Detrimental effects of a failed infection by a co-invasive parasite on a native congeneric parasite and its native host

McIntire, Kristina M.; Juliano, Steven A.

doi:10.1007/s10530-021-02464-0

Cited by 4 publications

(5 citation statements)

References 61 publications

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“…Our data showed that in squirrels of both sexes, the probability of surviving over the next twelve months was negatively related to S. robustus egg counts, indicating a negative effect of the alien parasite on local red squirrel survival. It is widely assumed that spillover of an alien parasite from an invading to a closely-related native species will be severely detrimental to the new host, because the naïve species will represent a physiologically similar host, but lack any coevolved tolerance or resistance to the parasite (Prenter et al 2004;Strauss et al 2012;McIntire and Juliano 2021). However, despite such host-switching events appear to be relatively common in biological invasions, studies demonstrating the pathogenic effect of alien macroparasites on native animal hosts, particularly mammals, are surprisingly few and only in a handful of cases the impact on naïve hosts was found to be higher than on the natural host, supporting the occurrence of parasite-mediated competition (see Lymbery et al 2014 and references therein).…”

Section: Discussionmentioning

confidence: 99%

“…However, invading hosts will likely introduce at least some parasite species from their native range and these alien parasites may spill-over to a susceptible native species (Power and Mitchell 2004;Telfer and Bown 2012). It is widely assumed that such shared parasites may then mediate the competition between the two species: if the alien parasite has a greater impact on the naïve species than on the invader, the latter will gain a competitive advantage and the probability of a successful invasion will increase (disease-mediated invasions) (Strauss et al 2012;McIntire and Juliano 2021). Finally, alien species may also acquire local parasites, amplifying (spillback: Kelly et al 2009;Sherrard-Smith et al 2015) or diluting their circulation (dilution effect: Thieltges et al 2009;Telfer and Brown 2012).…”

Section: Introductionmentioning

confidence: 99%

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Invading parasites: spillover of an alien nematode reduces survival in a native species

et al. 2021

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It is widely assumed that spillover of alien parasites to native host species severely impacts naïve populations, ultimately conferring a competitive advantage to invading hosts that introduced them. Despite such host-switching events occurring in biological invasions, studies demonstrating the impact of alien macroparasites on native animal hosts are surprisingly few. In Europe, native red squirrels (Sciurus vulgaris) are replaced by introduced North American grey squirrels (S. carolinensis) mainly through resource competition, and, only in the United Kingdom and Ireland, by competition mediated by a viral disease. In Italy such disease is absent, but spillover of an introduced North American nematode (Strongyloides robustus) from grey to red squirrels is known to occur. Here, we used long-term (9 years) capture-mark-recapture and parasitological data of red squirrels in areas co-inhabited by grey squirrels in Northern Italy to investigate the impact of this alien helminth on naïve native squirrels’ body mass, local survival, and reproduction of females. We found no negative effect of the alien parasite on body mass or reproductive success, but intensity of infection by S. robustus reduced survival of both male and female squirrels. Significantly, survival of squirrels co-infected by their native nematode, Trypanoxyuris sciuri, was less affected by S. robustus, suggesting a protective effect of the native helminth against the new infection. Hence, we demonstrate that alien S. robustus spillover adds to the detrimental effects of resource competition and stress induced by grey squirrels, further reducing the fitness of the native species in the presence of the invasive competitor.

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Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Invading parasites: spillover of an alien nematode reduces survival in a native species

et al. 2021

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“…Oocyst prevalence and abundance in the water were quantified (Fellous and Koella 2009, McIntire and Juliano 2021), yielding our measures of oocyst prevalence (proportion of adults and deceased pupae bearing oocysts) and oocyst infection intensity (oocysts per infected adult or deceased pupa). Oocyst production for individuals that died as pupae was included in this analysis, as late pupal death can result in successful completion of the parasite life cycle (Chen 1999).…”

Section: Methodsmentioning

confidence: 99%

How do noncompetent hosts cause dilution of parasitism? Testing hypotheses for native and invasive mosquitoes

McIntire

Chappell

Juliano

2021

Ecology

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Parasite dilution occurs in varied systems, via multiple potential mechanisms. We used laboratory manipulation and field surveys to test for invader‐induced parasite dilution via two specific mechanisms: host–host competition and encounter reduction. In the laboratory, single Aedes triseriatus larvae were exposed to one of eight combinations of: parasitic Ascogregarina barretti, +/−1 cohabiting Aedes albopictus larva during parasite exposure, and +/−1 cohabiting A. albopictus larva after infectious parasite removal. Larval infection intensity (predicted to decrease via dilution by encounter reduction) was not significantly affected by A. albopictus. Adult infection prevalence and intensity (predicted to decrease via dilution by host–host competition) were significantly greater with A. albopictus, suggesting parasite amplification by interspecific competition, an effect potentially mediated by competition increasing A. triseriatus development time. In the field, we tested for effects of potential dilution host abundances on prevalence and abundance of A. barretti in A. triseriatus larvae. Piecewise path analysis yielded no evidence of host–host competition impacting parasitism in the field, but instead indicated a significant direct negative effect of Aedes spp. abundance on parasite abundance in A. triseriatus, which is consistent with dilution via encounter reduction in the field, but only in tree holes, not in man‐made containers. Our results are consistent with the hypothesis that a noncompetent invader can alter the native host–parasite relationship, but our laboratory and field data yield differing results. This difference is likely due to laboratory experiment testing for per capita effects of dilution hosts on parasitism, but field analysis testing for effects of dilution host abundance on parasitism. Individually, host–host competition with the invader amplifies, rather than dilutes, parasite success. In contrast, our path analysis is consistent with the hypothesis that dilution of parasitism results from increased abundance of noncompetent hosts in the field.

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“…Environmental variables within a parasite's invasive range may impact its growth and life cycle, and thereby influence how parasites affect their novel hosts (e.g., Cline et al 2014;Liu et al 2021). Novel hosts exert unique selection pressures on invasive parasites that may lead to altered host-parasite dynamics (Telfer and Bown 2012;McIntire and Juliano 2021) via shifts in parasite strategy and population genetic structure (Brown et al 2009;Emde et al 2014;Beaurepaire et al 2019). Long-term studies of parasite invasions are critical for identifying evolutionary changes within introduced populations, which may be consequential for the conservation and survival of vulnerable host species.…”

Section: Introductionmentioning

confidence: 99%

“…Previous studies have found that P. downsi shows little evidence for genetic differentiation across five islands in the Galápagos archipelago (Santa Cruz, Floreana, Isabela, Santiago and San Cristobal) and across the lowland and highland habitats (Dudaniec et al 2008a;Koop et al 2020), indicative of moderate to high genetic dispersal. However, given strong selection pressures associated with invasion (Le Roux 2021), genetic drift in small founding populations (Polechová 2018), and interactions with multiple novel hosts (Telfer and Bown 2012;McIntire and Juliano 2021), P. downsi is expected to show evolutionary shifts since its introduction. Further, previous research detected morphological changes in P. downsi, with an ~ 11% decrease in female body length and a ~ 26% decrease in female abdomen size between 2004-2016, the latter trait being strongly correlated with fecundity (Common et al 2020).…”

Section: Introductionmentioning

confidence: 99%

Genetics reveals shifts in reproductive behaviour of the invasive bird parasite Philornis downsi collected from Darwin’s finch nests

et al. 2022

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Due to novel or dynamic fluctuations in environmental conditions and resources, host and parasite relationships can be subject to diverse selection pressures that may lead to significant changes during and after invasion of a parasite. Genomic analyses are useful for elucidating evolutionary processes in invasive parasites following their arrival to a new area and host. Philornis downsi (Diptera: Muscidae), the avian vampire fly, was introduced to the Galápagos Islands circa 1964 and has since spread across the archipelago, feeding on the blood of developing nestlings of endemic land birds. Since its discovery, there have been significant changes to the dynamics of P. downsi and its novel hosts, such as shifting mortality rates and changing oviposition behaviour, however no temporal genetic studies have been conducted. We collected P. downsi from nests and traps from a single island population over a 14-year period, and genotyped flies at 469 single nucleotide polymorphisms (SNPs) using restriction-site associated DNA sequencing (RADSeq). Despite significant genetic differentiation (FST) between years, there was no evidence for genetic clustering within or across four sampling years between 2006 and 2020, suggesting a lack of population isolation. Sibship reconstructions from P. downsi collected from 10 Darwin’s finch nests sampled in 2020 showed evidence for shifts in reproductive behaviour compared to a similar genetic analysis conducted in 2004–2006. Compared with this previous study, females mated with fewer males, individual females oviposited fewer offspring per nest, but more unique females oviposited per nest. These findings are important to consider within reproductive control techniques, and have fitness implications for both parasite evolution and host fitness.

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Detrimental effects of a failed infection by a co-invasive parasite on a native congeneric parasite and its native host

Cited by 4 publications

References 61 publications

Invading parasites: spillover of an alien nematode reduces survival in a native species

Invading parasites: spillover of an alien nematode reduces survival in a native species

How do noncompetent hosts cause dilution of parasitism? Testing hypotheses for native and invasive mosquitoes

Genetics reveals shifts in reproductive behaviour of the invasive bird parasite Philornis downsi collected from Darwin’s finch nests

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