Lieven Therry

Variation in innate immunity in relation to ectoparasite load, age and season: a field experiment in great tits (Parus major)

SUMMARY It remains largely unknown which factors affect the innate immune responses of free-living birds. Nevertheless, the degree of innate immunity may play a crucial role in an individuals survival as it procures the first defence against pathogens. We manipulated the ectoparasite load of great tit (Parus major) nests by infesting them with hen fleas (Ceratophyllus gallinae) before egg laying. We subsequently quantified natural antibody (NAb) concentration and complement activation in nestlings and adult females during breeding and post-breeding periods. NAb concentrations increased in nestlings and adult females breeding in flea-infested nest boxes during the nestling provisioning period, but not in breeding females during incubation. In contrast, parasite abundance did not affect levels of complement activity in females. NAb levels of nestlings were already fully developed at the end of the nestling stage, but complement activation was only observed post-fledging. Concentrations of NAbs and complement activation of adult females were significantly lower during the breeding season compared with post-breeding levels, but did not differ between incubation and chick rearing. Further experimental studies in species that vary in life-history strategies will allow us to unravel the mechanisms underlying the observed variation in innate immune defences.

Rapid range expansion increases genetic differentiation while causing limited reduction in genetic diversity in a damselfly

Many ectothermic species are currently expanding their geographic range due to global warming. This can modify the population genetic diversity and structure of these species because of genetic drift during the colonization of new areas. Although the genetic signatures of historical range expansions have been investigated in an array of species, the genetic consequences of natural, contemporary range expansions have received little attention, with the only studies available focusing on range expansions along a narrow front. We investigate the genetic consequences of a natural range expansion in the Mediterranean damselfly Coenagrion scitulum, which is currently rapidly expanding along a broad front in different directions. We assessed genetic diversity and genetic structure using 12 microsatellite markers in five centrally located populations and five recently established populations at the edge of the geographic distribution. Our results suggest that, although a marginal significant decrease in the allelic richness was found in the edge populations, genetic diversity has been preserved during the range expansion of this species. Nevertheless, edge populations were genetically more differentiated compared with core populations, suggesting genetic drift during the range expansion. The smaller effective population sizes of the edge populations compared with central populations also suggest a contribution of genetic drift after colonization. We argue and document that range expansion along multiple axes of a broad expansion front generates little reduction in genetic diversity, yet stronger differentiation of the edge populations.

Rapid evolution of larval life history, adult immune function and flight muscles in a poleward-moving damselfly.

Although a growing number of studies have documented the evolution of adult dispersal‐related traits at the range edge of poleward‐expanding species, we know little about evolutionary changes in immune function or traits expressed by nondispersing larvae. We investigated differentiation in larval (growth and development) and adult traits (immune function and flight‐related traits) between replicated core and edge populations of the poleward‐moving damselfly Coenagrion scitulum. These traits were measured on individuals reared in a common garden experiment at two different food levels, as allocation trade‐offs may be easier to detect under energy shortage. Edge individuals had a faster larval life history (growth and development rates), a higher adult immune function and a nearly significant higher relative flight muscle mass. Most of the differentiation between core and edge populations remained and edge populations had a higher relative flight muscle mass when corrected for latitude‐specific thermal regimes, and hence could likely be attributed to the range expansion process per se. We here for the first time document a higher immune function in individuals at the expansion front of a poleward‐expanding species and documented the rarely investigated evolution of faster life histories during range expansion. The rapid multivariate evolution in these ecological relevant traits between edge and core populations is expected to translate into changed ecological interactions and therefore has the potential to generate novel eco‐evolutionary dynamics at the expansion front.

Neutral and adaptive genomic signatures of rapid poleward range expansion

Many species are expanding their range polewards, and this has been associated with rapid phenotypic change. Yet, it is unclear to what extent this reflects rapid genetic adaptation or neutral processes associated with range expansion, or selection linked to the new thermal conditions encountered. To disentangle these alternatives, we studied the genomic signature of range expansion in the damselfly Coenagrion scitulum using 4950 newly developed genomic SNPs and linked this to the rapidly evolved phenotypic differences between core and (newly established) edge populations. Most edge populations were genetically clearly differentiated from the core populations and all were differentiated from each other indicating independent range expansion events. In addition, evidence for genetic drift in the edge populations, and strong evidence for adaptive genetic variation in association with the range expansion was detected. We identified one SNP under consistent selection in four of the five edge populations and showed that the allele increasing in frequency is associated with increased flight performance. This indicates collateral, non‐neutral evolutionary changes in independent edge populations driven by the range expansion process. We also detected a genomic signature of adaptation to the newly encountered thermal regimes, reflecting a pattern of countergradient variation. The latter signature was identified at a single SNP as well as in a set of covarying SNPs using a polygenic multilocus approach to detect selection. Overall, this study highlights how a strategic geographic sampling design and the integration of genomic, phenotypic and environmental data can identify and disentangle the neutral and adaptive processes that are simultaneously operating during range expansions.

Sexual selection on flight endurance, flight-related morphology and physiology in a scrambling damselfly

We have limited knowledge on the mechanistic base of sexual selection, especially in scrambling species. This asks for a functional approach that explores the link between each component of the phenotype-performance-fitness axis and that includes both morphological and physiological traits. We explored the phenotype-performance-fitness axis in the scrambling damselfly Coenagrion puella by studying the links between a set of physiological and morphological traits, flight performance (flight speed and flight endurance), and short-term mating success. As expected for scrambling competition, there was sexual selection for increased flight endurance rather than for increased flight speed. For fat content, we could demonstrate the full phenotype-performance-fitness axis, where selection for a higher fat content could be explained by the sexual selection for a higher flight endurance and the positive covariation between fat content and flight endurance. For three other traits (size, relative flight muscle mass and wing loading), however, we detected selection that could not be explained via their effect on flight performance, generating novel testable hypotheses about how the covariation between these traits and mating success is generated. This also urges caution when using morphological traits as proxies for flight speed and flight endurance in phenotypic selection studies.

Rapid evolution of increased vulnerability to an insecticide at the expansion front in a poleward-moving damselfly

Many species are too slow to track their poleward‐moving climate niche under global warming. Pesticide exposure may contribute to this by reducing population growth and impairing flight ability. Moreover, edge populations at the moving range front may be more vulnerable to pesticides because of the rapid evolution of traits to enhance their rate of spread that shunt energy away from detoxification and repair. We exposed replicated edge and core populations of the poleward‐moving damselfly Coenagrion scitulum to the pesticide esfenvalerate at low and high densities. Exposure to esfenvalerate had strong negative effects on survival, growth rate, and development time in the larval stage and negatively affected flight‐related adult traits (mass at emergence, flight muscle mass, and fat content) across metamorphosis. Pesticide effects did not differ between edge and core populations, except that at the high concentration the pesticide‐induced mortality was 17% stronger in edge populations. Pesticide exposure may therefore slow down the range expansion by lowering population growth rates, especially because edge populations suffered a higher mortality, and by negatively affecting dispersal ability by impairing flight‐related traits. These results emphasize the need for direct conservation efforts toward leading‐edge populations for facilitating future range shifts under global warming.

Unravelling the effects of contemporary and historical range expansion on the distribution of genetic diversity in the damselfly Coenagrion scitulum

Although genetic diversity provides the basic substrate for evolution, there are a limited number of studies that assess the impact of recent climate change on intraspecific genetic variation. This study aims to unravel the degree to which historical and contemporary factors shape genetic diversity and structure across a large part of the range of the range‐expanding damselfly Coenagrion scitulum (Rambur, 1842). A total of 525 individuals from 31 populations were genotyped at nine microsatellites, and a subset was sequenced at two mitochondrial genes. We inferred the importance of geography, environmental factors, and recent range expansion on genetic diversity and structure. Genetic diversity decreased going westwards, suggesting a signature of historical post‐glacial expansion from east to west and the presence of eastern refugia. Although genetic differentiation decreased going northwards, it increased in the northern edge populations, suggesting a role of contemporary range expansion on the genetic make‐up of populations. The phylogeographical context was proven to be essential in understanding and identifying the genetic signatures of local contemporary processes. Within this framework, our results highlight that recent range expansion of a good disperser can decrease genetic diversity and increase genetic differentiation which should be considered when devising suitable conservation strategies.

Delayed effects of chlorpyrifos across metamorphosis on dispersal-related traits in a poleward moving damselfly

How exposure to contaminants may interfere with the widespread poleward range expansions under global warming is largely unknown. Pesticide exposure may negatively affect traits shaping the speed of range expansion, including traits related to population growth rate and dispersal-related traits. Moreover, rapid evolution of growth rates during poleward range expansions may come at a cost of a reduced investment in detoxification and repair thereby increasing the vulnerability to contaminants at expanding range fronts. We tested effects of a sublethal concentration of the widespread pesticide chlorpyrifos on traits related to range expansion in replicated edge and core populations of the poleward moving damselfly Coenagrion scitulum reared at low and high food levels in a common garden experiment. Food limitation in the larval stage had strong negative effects both in the larval stage and across metamorphosis in the adult stage. Exposure to chlorpyrifos during the larval stage did not affect larval traits but caused delayed effects across metamorphosis by increasing the incidence of wing malformations during metamorphosis and by reducing a key component of the adult immune response. There was some support for an evolutionary trade-off scenario as the faster growing edge larvae suffered a higher mortality during metamorphosis. Instead, there was no clear support for the faster growing edge larvae being more vulnerable to chlorpyrifos. Our data indicate that sublethal delayed effects of pesticide exposure, partly in association with the rapid evolution of faster growth rates, may slow down range expansions.

Higher investment in flight morphology does not trade off with fecundity estimates in a poleward range‐expanding damselfly

1. Evolutionary increases in dispersal‐related traits are frequently documented during range expansions. Investment in flight‐related traits is energetically costly and a trade‐off with fecundity may be expected during range expansion.

New records of host-parasite relationships between Coenagrion scitulum (Rambur, 1842) (Odonata) and water mite larvae (Hydrachnidia) in core and edge host populations

The relationships between water mite larvae parasitizing Coenagrion scitulum in core and edge populations were described. A total of 636 larvae of 7 water mite species were found on 143 C. scitulum adults (82 females and 61 males). C. scitulum was recorded for the first time as a host species for Arrenurus cuspidator, A. bruzelii, A. bicuspidator, A. tricuspidator, A. claviger and Hydryphantes octoporus. The degree of infestation by particular parasite species was typical for these species. In contrast, the parasites’ preferences for host body parts were not typical, as they preferred abdominal segments 2–4, which in earlier studies had been avoided by water mite larvae. No differences were found in degree of infestation of Coenagrion scitulum individuals between core and edge populations, with the exception of Hydryphantes octoporus, which parasitized damselflies only in core populations.