Understanding the joint evolution of dispersal and host specialisation using phytophagous arthropods as a model group.

Theory generally predicts that host specialisation and dispersal should evolve jointly. Indeed, many models predict that specialists should be poor dispersers to avoid landing on unsuitable hosts while generalists will have high dispersal abilities. Phytophagous arthropods are an excellent group to test this prediction, given extensive variation in their host range and dispersal abilities. Here, we explore the degree to which the empirical literature on this group is in accordance with theoretical predictions. We first briefly outline the theoretical reasons to expect such a correlation. We then report empirical studies that measured both dispersal and the degree of specialisation in phytophagous arthropods. We find a correlation between dispersal and levels of specialisation in some studies, but with wide variation in this result. We then review theoretical attributes of species and environment that may blur this correlation, namely environmental grain, temporal heterogeneity, habitat selection, genetic architecture, and coevolution between plants and herbivores. We argue that theoretical models fail to account for important aspects, such as phenotypic plasticity and the impact of selective forces stemming from other biotic interactions, on both dispersal and specialisation. Next, we review empirical caveats in the study of this interplay. We find that studies use different measures of both dispersal and specialisation, hampering comparisons. Moreover, several studies do not provide independent measures of these two traits. Finally, variation in these traits may occur at scales that are not being considered. We conclude that this correlation is likely not to be expected from large-scale comparative analyses as it is highly context dependent and should not be considered in isolation from the factors that modulate it, such as environmental scale and heterogeneity, intrinsic traits or biotic interactions. A stronger crosstalk between theoretical and empirical studies is needed to understand better the prevalence and basis of the correlation between dispersal and specialisation.

Ivermectin decreases parasite load, testosterone, and potentially antler length in a group of captive red deer males (Cervus elaphus).

Secondary sex traits (SSTs) can favour males in intra-sexual competition, allowing females to reliably assess their quality. They can also be connected to other aspects of fitness, such as resistance to parasites and pathogens, as parasites have negative effects on the development of SSTs. Antlers are one of the most recognizable examples of SSTs whose development is regulated by testosterone and reflects the actual condition of the bearer. Elevated testosterone can exaggerate the size of SSTs while impairing the function of the immune system ("The Immunocompetence Handicap Hypothesis") posing a trade-off between antler development and immune function. In this study, we experimentally manipulated the parasite load in captive red deer (Cervus elaphus) males with Ivermectin during antler development for two consecutive years. Expecting an inverse proportionality between parasite load and antler size, we hypothesized the treated deer to have larger antlers than the untreated ones. Our results showed that, following the immunocompetence handicap hypothesis, parasite load was positively associated with testosterone levels. However, the application of Ivermectin suppressed the parasite load of the treated animals but did not lead to the development of larger antlers. Instead, it significantly suppressed the concentration of testosterone in the treated animals, whilst the animals that had higher testosterone also had the highest parasite load. Our findings show that Ivermectin can potentially decrease the levels of testosterone and, consequently, antler size. These findings have important implications for the management of captive populations, especially in contexts where the development of large trophies is desired.

Integration of the immune memory into the pathogen-driven MHC polymorphism hypothesis.

Major histocompatibility complex (MHC) genes (referred to as human leukocyte antigen or HLA in humans) are a key component of vertebrate immune systems, coding for proteins which present antigens to T-cells. These genes are outstanding in their degree of polymorphism, with important consequences for human and animal health. The polymorphism is thought to arise from selection pressures imposed by pathogens on MHC allomorphs, which differ in their antigen-binding capacity. However, the existing theory has not considered MHC selection in relation to the formation of immune memory. In this paper, we argue that this omission limits our understanding of the evolution of MHC polymorphism and its role in disease. We review recent evidence that has emerged from the massive research effort related to the SARS-CoV-2 pandemics, and which provides new evidence for the role of MHC in shaping immune memory. We then discuss why the inclusion of immune memory within the existing theory may have non-trivial consequence for our understanding of the evolution of MHC polymorphism. Finally, we will argue that neglecting immune memory hinders our interpretation of empirical findings, and postulate that future studies focusing on pathogen-driven MHC selection would benefit from stratifying the available data according to the history of infection (and vaccination, if relevant).

Sexually selected male weapon increases the risk of population extinction under environmental change: an experimental evidence.

Exaggerated sexually selected traits (SSTs), occurring more commonly in males, help individuals to increase reproductive success but are costly to produce and maintain. These costs on the one hand may improve population fitness by intensifying selection against maladapted males, but on the other hand, may increase the risk of extinction under environmental challenges. However, the impact of SSTs on extinction risk has not been investigated experimentally. We used replicate populations of a male-dimorphic mite, Rhizoglyphus robini, to test if the prevalence of a sexually selected weapon affected the risk of extinction under temperature increase (TI) (2°C per each of three consecutive generations). In two independent experiments that utilized either inbred lines or lines mass selected for or against the weapon to establish experimental replicate populations differing in the prevalence of the weapon, we found that populations with high weapon prevalence were more likely to go extinct. Extinctions occurred despite partial suppression of the weapon expression at increased temperature and were not explained by increased male mortality. Our results provide the first, to our knowledge, experimental evidence demonstrating the dramatic effect of elaborated sexual traits on the risk of extinction under environmental challenges.

Small-scale genetic structure of populations of the bulb mite Rhizoglyphus robini.

Bulb mites are an economically significant pest of subterranean parts of plants and a versatile laboratory animal. However, the genetic structure of their populations remains unknown. To fill this gap in our knowledge of their biology, we set up a field experiment in which we allowed mites to colonize onion bulbs, and then determined the genetic structure of colonisers based on a panel of microsatellite loci. We found moderate but significant population structure among sites separated by ca. 20 m (FST range 0.03-0.21), with 7% of genetic variance distributed among sites. Allelic richness within some bulbs was nearly as high as that in the total population, suggesting that colonisation of bulbs was not associated with strong population bottlenecks. The significant genetic structure we observed over small spatial scales seems to reflect limited dispersal of mites in soil.

The quest for good genes: Epigamic traits, fitness, MHC and multilocus heterozygosity in the guppy.

The 'good genes' hypothesis for the evolution of male secondary sexual traits poses that female preferences for such traits are driven by indirect genetic benefits. However, support for the hypothesis remains ambiguous, and, in particular, the genetic basis for the benefits has rarely been investigated. Here, we use seminatural populations of Trinidadian guppies to investigate whether sexually selected traits (orange, black and iridescent colouration, gonopodium length and body size) predict fitness measured as the number of grandoffspring, a metric that integrates across fitness components and sexes. Furthermore, we tested whether two potential sources of genetic benefits-major histocompatibility complex (MHC) genotypes and multilocus heterozygosity (MLH)-are significant predictors of fitness and of the size of sexually selected traits. We found a significant, nonlinear effect of the area of black pigmentation and male body size on the number of grandoffspring, suggesting stabilizing selection on black area, and nonlinear selection favouring small body size. MLH was heritable (h2 = 0.14) and significantly predicted the number of grandoffspring, indicating the potential for genetic benefits based on heterozygosity. We also found support for local heterozygosity effects, which may reflect a noneven distribution of genetic load across the genome. MHC genotype was not significantly associated with any tested fitness component, or with the load of Gyrodactylus parasites. Neither MHC nor MLH was significant predictor of sexually selected traits. Overall, our results highlight the role of heterozygosity in determining fitness, but do not provide support for male sexually selected traits being indicators of genetic quality.

A sexually selected male weapon characterized by strong additive genetic variance and no evidence for sexually antagonistic polyphenic maintenance.

Sexual selection and sexual antagonism are important drivers of eco-evolutionary processes. The evolution of traits shaped by these processes depends on their genetic architecture, which remains poorly studied. Here, implementing a quantitative genetics approach using diallel crosses of the bulb mite, Rhizoglyphus robini, we investigated the genetic variance that underlies a sexually selected weapon that is dimorphic among males and female fecundity. Previous studies indicated that a negative genetic correlation between these two traits likely exists. We found male morph showed considerable additive genetic variance, which is unlikely to be explained solely by mutation-selection balance, indicating the likely presence of large-effect loci. However, a significant magnitude of inbreeding depression also indicates that morph expression is likely to be condition-dependent to some degree and that deleterious recessives can simultaneously contribute to morph expression. Female fecundity also showed a high degree of inbreeding depression, but the variance in female fecundity was mostly explained by epistatic effects, with very little contribution from additive effects. We found no significant genetic correlation, nor any evidence for dominance reversal, between male morph and female fecundity. The complex genetic architecture underlying male morph and female fecundity in this system has important implications for our understanding of the evolutionary interplay between purifying selection and sexually antagonistic selection.

Effective specialist or jack of all trades? Experimental evolution of a crop pest in fluctuating and stable environments.

Understanding pest evolution in agricultural systems is crucial for developing effective and innovative pest control strategies. Types of cultivation, such as crop monocultures versus polycultures or crop rotation, may act as a selective pressure on pests' capability to exploit the host's resources. In this study, we examined the herbivorous mite Aceria tosichella (commonly known as wheat curl mite), a widespread wheat pest, to understand how fluctuating versus stable environments influence its niche breadth and ability to utilize different host plant species. We subjected a wheat-bred mite population to replicated experimental evolution in a single-host environment (either wheat or barley), or in an alternation between these two plant species every three mite generations. Next, we tested the fitness of these evolving populations on wheat, barley, and on two other plant species not encountered during experimental evolution, namely rye and smooth brome. Our results revealed that the niche breadth of A. tosichella evolved in response to the level of environmental variability. The fluctuating environment expanded the niche breadth by increasing the mite's ability to utilize different plant species, including novel ones. Such an environment may thus promote flexible host-use generalist phenotypes. However, the niche expansion resulted in some costs expressed as reduced performances on both wheat and barley as compared to specialists. Stable host environments led to specialized phenotypes. The population that evolved in a constant environment consisting of barley increased its fitness on barley without the cost of utilizing wheat. However, the population evolving on wheat did not significantly increase its fitness on wheat, but decreased its performance on barley. Altogether, our results indicated that, depending on the degree of environmental heterogeneity, agricultural systems create different conditions that influence pests' niche breadth evolution, which may in turn affect the ability of pests to persist in such systems.

Genomic evidence that a sexually selected trait captures genome-wide variation and facilitates the purging of genetic load.

The evolution of costly traits such as deer antlers and peacock trains, which drove the formation of Darwinian sexual selection theory, has been suggested to both reflect and affect patterns of genetic variance across the genome, but direct tests are missing. Here, we used an evolve and resequence approach to reveal patterns of genome-wide diversity associated with the expression of a sexually selected weapon that is dimorphic among males of the bulb mite, Rhizoglyphus robini. Populations selected for the weapon showed reduced genome-wide diversity compared to populations selected against the weapon, particularly in terms of the number of segregating non-synonymous positions, indicating enhanced purifying selection. This increased purifying selection reduced inbreeding depression, but outbred female fitness did not improve, possibly because any benefits were offset by increased sexual antagonism. Most single nucleotide polymorphisms (SNPs) that consistently diverged in response to selection were initially rare and overrepresented in exons, and enriched in regions under balancing or relaxed selection, suggesting they are probably moderately deleterious variants. These diverged SNPs were scattered across the genome, further demonstrating that selection for or against the weapon and the associated changes to the mating system can both capture and influence genome-wide variation.

Long term patterns of association between MHC and helminth burdens in the bank vole support Red Queen dynamics.

Major histocompatibility complex (MHC) genes encode proteins crucial for adaptive immunity of vertebrates. Negative frequency-dependent selection (NFDS), resulting from adaptation of parasites to common MHC types, has been hypothesized to maintain high, functionally relevant polymorphism of MHC, but demonstration of this relationship has remained elusive. In particular, differentiation of NFDS from fluctuating selection, resulting from changes in parasite communities in time and space (FS), has proved difficult in short-term studies. Here, we used temporal data, accumulated through long-term monitoring of helminths infecting bank voles (Myodes glareolus), to test specific predictions of NFDS on MHC class II. Data were collected in three, moderately genetically differentiated subpopulations in Poland, which were characterized by some stable spatiotemporal helminth communities but also events indicating introduction of new species and loss of others. We found a complex association between individual MHC diversity and species richness, where intermediate numbers of DRB supertypes correlated with lowest species richness, but the opposite was true for DQB supertypes-arguing against universal selection for immunogenetic optimality. We also showed that particular MHC supertypes explain a portion of the variance in prevalence and abundance of helminths, but this effect was subpopulation-specific, which is consistent with both NFDS and FS. Finally, in line with NFDS, we found that certain helminths that have recently colonized or spread in a given subpopulation, more frequently or intensely infected voles with MHC supertypes that have been common in the recent past. Overall, our results highlight complex spatial and temporal patterns of MHC-parasite associations, the latter being consistent with Red Queen coevolutionary dynamics.

What do orange spots reveal about male (and female) guppies? A test using correlated responses to selection.

Female preferences for male ornamental traits can arise from indirect benefits, such as increased attractiveness or better viability of progeny, but empirical evidence for such benefits is inconsistent. Artificial selection offers a powerful way to investigate indirect effects of male ornaments. Here, we selected for the area of orange spots on male guppies, a trait subject to female preferences in our population, in replicated up- and down-selected lines. We found a significant direct response to selection, and a correlated response in female preferences, with females from down-selected lines showing less interest in more orange males. Nevertheless, up-selected males sired more offspring in direct competition with low-selected males, irrespective of female origin. We did not find a significantly correlated response to selection among any other fitness correlates we measured. Our results imply that female preferences for orange spots can lead to increased reproductive success of their sons, with no effect on general viability of progeny. Furthermore, although we demonstrate that female preferences may evolve via linkage disequilibrium with the preferred trait, the potential for runaway selection by positive feedback may be constrained by the lack of corresponding linkage with male reproductive competitiveness.

Functional immunogenetic variation, rather than local adaptation, predicts ectoparasite infection intensity in a model fish species.

Natural host populations differ in their susceptibility to infection by parasites, and these intrapopulation differences are still an incompletely understood component of host-parasite dynamics. In this study, we used controlled infection experiments with wild-caught guppies (Poecilia reticulata) and their ectoparasite Gyrodactylus turnbulli to investigate the roles of local adaptation and host genetic composition (immunogenetic and neutral) in explaining differences in susceptibility to infection. We found differences between our four study host populations that were consistent between two parasite source populations, with no indication of local adaptation by either host or parasite at two tested spatial scales. Greater values of host population genetic variability metrics broadly aligned with lower population mean infection intensity, with the best alignments associated with major histocompatibility complex (MHC) "supertypes". Controlling for intrapopulation differences and potential inbreeding variance, we found a significant negative relationship between individual-level functional MHC variability and infection: fish carrying more MHC supertypes experienced infections of lower severity, with limited evidence for supertype-specific effects. We conclude that population-level differences in host infection susceptibility probably reflect variation in parasite selective pressure and/or host evolutionary potential, underpinned by functional immunogenetic variation.

Balancing selection versus allele and supertype turnover in MHC class II genes in guppies.

Selection pressure from parasites is thought to be a major force shaping the extreme polymorphism of the major histocompatibility complex (MHC) genes, but the modes and consequences of selection remain unclear. Here, we analyse MHC class II and microsatellite diversity in 16 guppy (Poecilia reticulata) populations from two islands (Trinidad and Tobago) that have been separated for at least 10 ky. Within-population MHC diversity was high, but allele sharing was limited within islands and even lower between islands, suggesting relatively fast turnover of alleles. Allelic lineages strongly supported in phylogenetic analyses tended to be island-specific, suggesting rapid lineage sorting, and an expansion of an allelic lineage private to Tobago was observed. New alleles appear to be generated locally at a detectably high frequency. We did not detect a consistent signature of local adaptation, but FST outlier analysis suggested that balancing selection may be the more general process behind spatial variation in MHC allele frequencies in this system, particularly within Trinidad. We found no evidence for divergent allele advantage within populations, or for decreased genetic structuring of MHC supertypes compared to MHC alleles. The dynamic and complex nature of MHC evolution we observed in guppies, coupled with some evidence for balancing selection shaping MHC allele frequencies, are consistent with Red Queen processes of host-parasite coevolution.

Expansion of frozen hybrids in the guppy ectoparasite, Gyrodactylus turnbulli.

Hybridization is one of the major factors contributing to the emergence of highly successful parasites. Hybrid vigour can play an important role in this process, but subsequent rounds of recombination in the hybrid population may dilute its effects. Increased fitness of hybrids can, however, be frozen by asexual reproduction. Here, we identify invasion of a 'frozen hybrid' genotype in natural populations of Gyrodactylus turnbulli, a facultatively sexual ectoparasitic flatworm that causes significant damage to its fish host. We resequenced genomes of these parasites infecting guppies from six Trinidad and Tobago populations, and found surprisingly high discrepancy in genome-wide nucleotide diversity between islands. The elevated heterozygosity on Tobago is maintained by predominantly clonal reproduction of hybrids formed from two diverged genomes. Hybridization has been followed by spread of the hybrids across the island, implying a selective advantage compared with native genotypes. Our results thus highlight that a single outcrossing event may be independently sufficient to cause pathogen expansion.

RNA-Seq analysis of the guppy immune response against Gyrodactylus bullatarudis infection.

Gyrodactylids are ubiquitous ectoparasites of teleost fish, but our understanding of the host immune response against them is fragmentary. Here, we used RNA-Seq to investigate genes involved in the primary response to infection with Gyrodactylus bullatarudis on the skin of guppies, Poecilia reticulata, an important evolutionary model, but also one of the most common fish in the global ornamental trade. Analysis of differentially expressed genes identified several immune-related categories, including IL-17 signalling pathway and Th17 cell differentiation, cytokine-cytokine receptor interaction, chemokine signalling pathway, NOD-like receptor signalling pathway, natural killer cell-mediated cytotoxicity and pathways involved in antigen recognition, processing and presentation. Components of both the innate and the adaptive immune responses play a role in response to gyrodactylid infection. Genes involved in IL-17/Th17 response were particularly enriched among differentially expressed genes, suggesting a significant role for this pathway in fish responses to ectoparasites. Our results revealed a sizable list of genes potentially involved in the teleost-gyrodactylid immune response.

Sexual and ecological selection on a sexual conflict gene.

Sexual selection and conflict can act on genes with important metabolic functions, potentially shaping standing genetic variance in such genes and thus evolutionary potential of populations. Here, using experimental evolution, we show how reproductive competition intensity and thermal environment affect selection on phosphogluconate dehydrogenase (6Pgdh)-a metabolic gene involved in sexual selection and conflict in the bulb mite. The S allele of 6Pgdh increases male success in reproductive competition, but is detrimental to S-bearing males' partners. We found that the rate of the S allele spread increased with the proportion of males in the experimental populations, illustrating that harm to females is more easily compensated for males under more intense sexual competition. Furthermore, we found that under equal sex ratio, the S allele spreads faster at higher temperature. While the direction of selection on 6Pgdh was not reversed in any of the conditions we tested, which would be required for environmental heterogeneity to maintain polymorphism at this locus, our study highlights that ecological and sexual selection can jointly affect selection on important metabolic enzymes.

Sexually selected male weapon is associated with lower inbreeding load but higher sex load in the bulb mite.

Elaborate sexually selected ornaments and armaments are costly but increase the reproductive success of their bearers (usually males). It has been postulated that high-quality males can invest disproportionately more in such traits, making those traits honest signals of genetic quality. However, genes associated with such traits may have sexually antagonistic effects on fitness. Here, using a bulb mite Rhizoglyphus robini, a species in which a distinct dimorphism exists between males in the expression of a sexually selected weapon, we compare inbreeding and gender load between lines derived from armed fighters and unarmed scramblers. After four generations of sib-mating, inbreeding depression for female fitness was significantly lower in fighter-derived lines compared to scrambler-derived lines, suggesting that fighter males had significantly higher genetic quality. However, outbred females from fighter-derived lines had significantly lower fitness compared to outbred females from scrambler-derived lines, demonstrating significant gender load associated with the presence of a sexually selected male weapon. Our results imply that under outbreeding, genetic benefits of mating with bearers of elaborate sexually selected traits might be swamped by the costs of decreased fitness of female progeny due to sexually antagonistic effects.

Gene duplications, divergence and recombination shape adaptive evolution of the fish ectoparasite Gyrodactylus bullatarudis.

Determining the molecular basis of parasite adaptation to its host is an important component in understanding host-parasite coevolution and the epidemiology of parasitic infections. Here, we investigate short- and long-term adaptive evolution in the eukaryotic parasite Gyrodactylus bullatarudis infecting Caribbean guppies (Poecilia reticulata), by comparing the reference genome of Tobagonian G. bullatarudis with other Platyhelminthes, and by analysing resequenced samples from local Trinidadian populations. At the macroevolutionary timescale, we observed duplication of G-protein and serine proteases genes, which are probably important in host-parasite arms races. Serine protease also showed strong evidence of ongoing, diversifying selection at the microevolutionary timescale. Furthermore, our analyses revealed that a hybridization event, involving two divergent genomes, followed by recombination has dramatically affected the genetic composition of Trinidadian populations. The recombinant genotypes invaded Trinidad and replaced local parasites in all populations. We localized more than 300 genes in regions fixed in local populations for variants of different origin, possibly due to diversifying selection pressure from local host populations. In addition, around 70 genes were localized in regions identified as heterozygous in some, but not all, individuals. This pattern is consistent with a very recent spread of recombinant parasites. Overall, our results are consistent with the idea that recombination between divergent genomes can result in particularly successful parasites.

Mating preferences can drive expansion or contraction of major histocompatibility complex gene family.

Major histocompatibility complex (MHC)-based mating rules can evolve as a way to avoid inbreeding or to increase offspring immune competence. While the role of mating preference in shaping the MHC diversity in vertebrates has been acknowledged, its impact on individual MHC diversity has not been considered. Here, we use computer simulations to investigate how simple mating rules favouring MHC-dissimilar partners affect the evolution of the number of MHC variants in individual genomes, accompanying selection for resistance to parasites. We showed that the effect of such preferences could sometimes be dramatic. If preferences are aimed at avoiding identical alleles, the equilibrium number of MHC alleles is much smaller than under random mating. However, if the mating rule minimizes the ratio of shared to different alleles in partners, MHC number is higher than under random mating. Additionally, our simulations revealed that a negative correlation between the numbers of MHC variants in mated individuals can arise from simple rules of MHC-disassortative mating. Our results reveal unexpected potential of MHC-based mating preferences to drive MHC gene family expansions or contractions and highlight the need to study the mechanistic basis of such preferences, which is currently poorly understood.