Annual environmental variation influences host tolerance to parasites.
ABSTRACT: When confronted with a parasite or pathogen, hosts can defend themselves by resisting or tolerating the attack. While resistance can be diminished when resources are limited, it is unclear how robust tolerance is to changes in environmental conditions. Here, we investigate the sensitivity of tolerance in a single host population living in a highly variable environment. We manipulated the abundance of an invasive parasitic fly, Philornis downsi, in nests of Galápagos mockingbirds ( Mimus parvulus) over four field seasons and measured host fitness in response to parasitism. Mockingbird tolerance to P. downsi varied significantly among years and decreased when rainfall was limited. Video observations indicate that parental provisioning of nestlings appears key to tolerance: in drought years, mockingbirds likely do not have sufficient resources to compensate for the effects of P. downsi. These results indicate that host tolerance is a labile trait and suggest that environmental variation plays a major role in mediating the consequences of host-parasite interactions.
Project description:Hybridization can increase adaptive potential when enhanced genetic diversity or novel genetic combinations confer a fitness advantage, such as in the evolution of anti-parasitic mechanisms. Island systems are especially susceptible to invasive parasites due to the lack of defence mechanisms that usually coevolve in long-standing host-parasite relationships. We test if host genetic admixture affects parasite numbers in a novel host-parasite association on the Galápagos Islands. Specifically, we compare the number of Philornis downsi in nests with offspring sired by Darwin's small tree finch (Camarhynchus parvulus), Darwin's medium tree finch (C. pauper) and hybrids of these two species. The number of P. downsi decreased with an increasing genetic admixture of the attending male, and nests of hybrid males had approximately 50% fewer parasites than C. parvulus nests, and approximately 60% fewer parasites than C. pauper nests. This finding indicates that hybridization in this system could be favoured by selection and reveal a mechanism to combat an invasive parasite.
Project description:Fecundity selection is a critical component of fitness and a major driver of adaptive evolution. Trade-offs between parasite mortality and host resources are likely to impose a selection pressure on parasite fecundity, but this is little studied in natural systems. The 'fecundity advantage hypothesis' predicts female-biased sexual size dimorphism whereby larger females produce more offspring. Parasitic insects are useful for exploring the interplay between host resource availability and parasite fecundity, because female body size is a reliable proxy for fecundity in insects. Here we explore temporal changes in body size in the myiasis-causing parasite Philornis downsi (Diptera: Muscidae) on the Galápagos Islands under conditions of earlier in-nest host mortality. We aim to investigate the effects of decreasing host resources on parasite body size and fecundity. Across a 12-year period, we observed a mean of c. 17% P. downsi mortality in host nests with 55 ± 6.2% host mortality and a trend of c. 66% higher host mortality throughout the study period. Using specimens from 116 Darwin's finch nests (Passeriformes: Thraupidae) and 114 traps, we found that over time, P. downsi pupae mass decreased by c. 32%, and male (c. 6%) and female adult size (c. 11%) decreased. Notably, females had c. 26% smaller abdomens in later years, and female abdomen size was correlated with number of eggs. Our findings imply natural selection for faster P. downsi pupation and consequently smaller body size and lower parasite fecundity in this newly evolving host-parasite system.
Project description:BACKGROUND:Understanding the dispersal and genetic structure of invasive insects across islands is important for designing management plans that are appropriate at spatial and temporal scales. For invasive parasites, population dynamics are largely determined by the distribution and density of their host species. The introduced parasitic fly, Philornis downsi, parasitises nestlings of endemic birds on all major islands of the Galápagos archipelago. The fly's high mortality and fitness impacts are of conservation concern for vulnerable and declining species of Darwin's finches. Using microsatellite data in Bayesian clustering and landscape genetic analyses, we examine gene flow and dispersal in P. downsi between three islands and across habitats (highlands, lowlands) and examine for the presence of population bottlenecks. We also examine variation at the mitochondrial gene CO1 across islands to establish if cryptic species were present. RESULTS:Both the mitochondrial and microsatellite data were consistent with there being a single species across islands. We found low genetic differentiation between islands and strong evidence for inter-island gene flow, or shared recent ancestry among individuals. Landscape genetic analysis identified two genetic clusters: one encompassing Santa Cruz and Isabela, and one on Floreana Island. There was no evidence of genetic differentiation between habitats and molecular variance was mainly attributable to within individuals. The combined P. downsi population was found to have undergone a population bottleneck. CONCLUSION:Philornis downsi populations have high connectivity within and between islands, with low levels of genetic differentiation between Floreana and the other two islands examined. The genetic bottleneck found across islands suggests there was a small founding population or few introduction events of P. downsi. The high dispersal capacity and wide habitat use of P. downsi highlights the significant threat that this parasite poses to the Galápagos avifauna. Our findings are relevant for assessing the viability of methods to control P. downsi on Galápagos, such as the sterile insect technique.
Project description:Introduced pathogens and other parasites are often implicated in host population level declines and extinctions. However, such claims are rarely supported by rigorous real-time data. Indeed, the threat of introduced parasites often goes unnoticed until after host populations have declined severely. The recent introduction of the parasitic nest fly, Philornis downsi, to the Galápagos Islands provides an opportunity to monitor the current impact of an invasive parasite on endemic land bird populations, including Darwin's finches.In this paper we present a population viability model to explore the potential long-term effect of P. downsi on Darwin's finch populations. The goal of our study was to determine whether P. downsi has the potential to drive host populations to extinction and whether management efforts are likely to be effective.Our model is based on data from five years of experimental field work documenting the effect of P. downsi on the reproductive success of medium ground finch Geospiza fortis populations on Santa Cruz Island. Under two of the three scenarios tested, the model predicted medium ground finches are at risk of extinction within the next century.However, sensitivity analyses reveal that even a modest reduction in the prevalence of the parasite could improve the stability of finch populations. We discuss the practicality of several management options aimed at achieving this goal.Synthesis and applications. Our study demonstrates the predicted high risk of local extinction of an abundant host species, the medium ground finch Geospiza fortis due to an introduced parasite, Philornis downsi. However, our study further suggests that careful management practices aimed at reducing parasite prevalence have the potential to significantly lower the risk of host species extinction.
Project description:Introduced parasites that alter their host's mating signal can change the evolutionary trajectory of a species through sexual selection. Darwin's Camarhynchus finches are threatened by the introduced fly Philornis downsi that is thought to have accidentally arrived on the Galapagos Islands during the 1960s. The P. downsi larvae feed on the blood and tissue of developing finches, causing on average approximately 55% in-nest mortality and enlarged naris size in survivors. Here we test if enlarged naris size is associated with song characteristics and vocal deviation in the small tree finch ( Camarhynchus parvulus), the critically endangered medium tree finch ( C. pauper) and the recently observed hybrid tree finch group ( Camarhynchus hybrids). Male C. parvulus and C. pauper with enlarged naris size produced song with lower maximum frequency and greater vocal deviation, but there was no significant association in hybrids. Less vocal deviation predicted faster pairing success in both parental species. Finally, C. pauper males with normal naris size produced species-specific song, but male C. pauper with enlarged naris size had song that was indistinguishable from other tree finches. When parasites disrupt host mating signal, they may also facilitate hybridization. Here we show how parasite-induced naris enlargement affects vocal quality, resulting in blurred species mating signals.
Project description:BACKGROUND: Parasites are evolutionary hitchhikers whose phylogenies often track the evolutionary history of their hosts. Incongruence in the evolutionary history of closely associated lineages can be explained through a variety of possible events including host switching and host independent speciation. However, in recently diverged lineages stochastic population processes, such as retention of ancestral polymorphism or secondary contact, can also explain discordant genealogies, even in fully co-speciating taxa. The relatively simple biogeographic arrangement of the Galápagos archipelago, compared with mainland biomes, provides a framework to identify stochastic and evolutionary informative components of genealogic data in these recently diverged organisms. RESULTS: Mitochondrial DNA sequences were obtained for four species of Galápagos mockingbirds and three sympatric species of ectoparasites--two louse and one mite species. These data were complemented with nuclear EF1? sequences in selected samples of parasites and with information from microsatellite loci in the mockingbirds. Mitochondrial sequence data revealed differences in population genetic diversity between all taxa and varying degrees of topological congruence between host and parasite lineages. A very low level of genetic variability and lack of congruence was found in one of the louse parasites, which was excluded from subsequent joint analysis of mitochondrial data. The reconciled multi-species tree obtained from the analysis is congruent with both the nuclear data and the geological history of the islands. CONCLUSIONS: The gene genealogies of Galápagos mockingbirds and two of their ectoparasites show strong phylogeographic correlations, with instances of incongruence mostly explained by ancestral genetic polymorphism. A third parasite genealogy shows low levels of genetic diversity and little evidence of co-phylogeny with their hosts. These differences can mostly be explained by variation in life-history characteristics, primarily host specificity and dispersal capabilities. We show that pooling genetic data from organisms living in close ecological association reveals a more accurate phylogeographic history for these taxa. Our results have implications for the conservation and taxonomy of Galápagos mockingbirds and their parasites.
Project description:Increasingly, multiple selective factors are recognized as jointly contributing to the evolution of morphology. What is not clear is how these forces vary across communities to promote morphological diversification among related species. In this study of Galápagos endemic snails (genus Naesiotus), we test several hypotheses of colour evolution. We observe mockingbirds (genus Mimus) predating live snails and find that avian predation selects against conspicuous shells. The evolutionary outcome of this selection is a diversity of shell colours across snails of the archipelago, each closely matching local backgrounds. We also find that snails more regularly exposed to the hot, equatorial sun reflect more light than shells of species from shadier habitats, suggesting a role for thermoregulatory constraints directing colour evolution. The signature of thermoregulatory selection is most clear in comparatively young communities (on the youngest islands), while the signature of selection from predators is most evident in older communities (on the older islands). Together, our findings point to a scenario of shifting selective forces along island ontogeny and community maturity that lead to the distribution of snail coloration we observe in Galápagos. Complex selective regimes such as these may have more responsibility for morphological diversity than is currently recognized.
Project description:Alien insect species may present a multifaceted threat to ecosystems into which they are introduced. In addition to the direct damage they may cause, they may also bring novel diseases and parasites and/or have the capacity to vector microorganisms that are already established in the ecosystem and are causing harm. Damage caused by ectoparasitic larvae of the invasive fly, Philornis downsi (Dodge and Aitken) to nestlings of endemic birds in the Galapagos Islands is well documented, but nothing is known about whether this fly is itself associated with parasites or pathogens. In this study, diagnostic molecular methods indicated the presence of insect trypanosomatids in P. downsi; to our knowledge, this is the first record of insect trypanosomatids associated with Philornis species. Phylogenetic estimates and evolutionary distances indicate these species are most closely related to the Crithidia and Blastocrithidia genera, which are not currently reported in the Galapagos Islands. The prevalence of trypanosomatids indicates either P. downsi arrived with its own parasites or that it is a highly suitable host for trypanosomatids already found in the Galapagos Islands, or both. We recommend further studies to determine the origin of the trypanosomatid infections to better evaluate threats to endemic fauna of the Galapagos Islands.
Project description:The invasive parasitic fly, Philornis downsi (Muscidae), is one of the greatest threats to the avifauna of the Galapagos Islands. The larvae of this fly feed on the blood and tissues of developing nestlings of at least 18 endemic and native birds. The aim of the current study was to investigate biotic and abiotic factors that may influence the population dynamics of this invasive parasite. To study the influence of vegetation zone and related climatic factors on fly numbers, a bi-weekly monitoring program using papaya-baited traps was carried out at a dry, lowland site and at a humid, highland site on Santa Cruz Island between 2012-2014. Female flies, a large proportion of which were inseminated and gravid, were collected throughout the year at both sites, indicating females were active during and between the bird breeding seasons. This is the first evidence that female flies are able to persist even when hosts are scarce. On the other hand, catch rates of male flies declined between bird breeding seasons. Overall, catch rates of P. downsi were higher in the drier, lowland habitat, which may be a consequence of host or resource availability. Time was a stronger predictor of adult fly numbers than climate, further suggesting that P. downsi does not appear to be limited by its environment, but rather by host availability. Seasonal catch rates suggested that populations in both habitats were continuous and multivoltine. Numbers of adult female flies appeared to be regulated chiefly by simple direct density dependence, and may be governed by availability of bird nests with nestlings. Nevertheless, confounding factors such as the existence of reservoir hosts that perpetuate fly populations and changes in behavior of P. downsi may increase the vulnerability of bird hosts that are already IUCN red-listed or in decline.
Project description:Parasite host range can be influenced by physiological, behavioral, and ecological factors. Combining data sets on host-parasite associations with phylogenetic information of the hosts and the parasites involved can generate evolutionary hypotheses about the selective forces shaping host range. Here, we analyzed associations between the nest-parasitic flies in the genus Philornis and their host birds on Trinidad. Four of ten Philornis species were only reared from one species of bird. Of the parasite species with more than one host bird species, P. falsificus was the least specific and P. deceptivus the most specific attacking only Passeriformes. Philornis flies in Trinidad thus include both specialists and generalists, with varying degrees of specificity within the generalists. We used three quantities to more formally compare the host range of Philornis flies: the number of bird species attacked by each species of Philornis, a phylogenetically informed host specificity index (Poulin and Mouillot's S TD), and a branch length-based S TD. We then assessed the phylogenetic signal of these measures of host range for 29 bird species. None of these measures showed significant phylogenetic signal, suggesting that clades of Philornis did not differ significantly in their ability to exploit hosts. We also calculated two quantities of parasite species load for the birds - the parasite species richness, and a variant of the S TD index based on nodes rather than on taxonomic levels - and assessed the signal of these measures on the bird phylogeny. We did not find significant phylogenetic signal for the parasite species load or the node-based S TD index. Finally, we calculated the parasite associations for all bird pairs using the Jaccard index and regressed these similarity values against the number of nodes in the phylogeny separating bird pairs. This analysis showed that Philornis on Trinidad tend to feed on closely related bird species more often than expected by chance.