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Magalhaes, S.

Publications and source records attributed to Magalhaes, S..

At least 19 recordsLinked to original sources

Unexpected changes in reproductive barriers between incipient species after experimental evolution in sympatry

Hybridization is generally considered a temporary phenomenon, but it is actually widespread and may last for large time periods between species that stably coexist. Here, to test whether evolving with a closely-related species modifies or maintains partial reproductive isolation, we performed experimental evolution in artificial sympatry vs. allopatry with two closely-related colour forms of spider mites (Tetranychus urticae) that exhibit an asymmetrical pattern of pre-mating isolation despite almost complete post-zygotic isolation. We assessed whether evolutionary changes occurred in traits associated to (i) pre-mating isolation, (ii) post-mating pre-zygotic and early post-zygotic isolation, and (iii) late post-zygotic isolation. Our results revealed that reinforcement did not occur even under forced long-term sympatric evolution. Instead, the strength of some reproductive barriers decreased (e.g., premating isolation and fertilization failure), and some trait changes indicated convergence rather than divergence between species (e.g., mating propensity, latency to copulation). In fact, both types of males showed the same decreased preference for red-form females across generations in sympatry. In line with this, traits underlying fertilization success evolved in the same direction and with similar amplitude in heterotypic crosses and in their homotypic control, as the offspring sex ratio of green-form females decreased in sympatry irrespective of the male they mated with. Finally, other changes in reproductive barriers resulted from trait correlations (e.g., decreased zygote mortality but increased juvenile mortality). Hence, despite very high costs of hybridization, responses occurring following evolution in sympatry were unrelated to selection directly associated to hybridization, but rather the by-product of other evolutionary forces, with cascading consequences for reproductive barriers. In particular, these results support the underappreciated hypothesis that within-species sexual interactions can constrain population diver-gence, or even drive trait convergence between species, thereby playing a role in the maintenance of partial reproductive isolation.

evolutionary biology↗

Spatiotemporal data integration for marine megafauna SDMs in dynamic environments: A point process approach

Species distribution models (SDMs) are widely used to predict where and when species occur, but the data available to fit them often resolve space and time unevenly. Designed surveys, such as line-transect distance-sampling surveys, provide structured spatial coverage and the detection information needed to estimate detectability, but logistical and funding constraints often limit them to short, infrequent periods. Opportunistic or citizen-science records are collected more frequently across the year, but from areas shaped by observer access and interest rather than survey design, and usually without comparable detection information. As a result, models built from either source alone tend to capture spatial structure or temporal dynamics well, but not both, limiting predictions for mobile species in dynamic environments. Here, we present a general framework, based on a log-Gaussian Cox process (LGCP) fitted using integrated nested Laplace approximations (INLA), that links multiple data sources to a shared spatiotemporal measure of species density through source-specific observation models: a detection function for survey transects, and spatial constraints reflecting the footprint of opportunistic effort. We apply the framework to cetacean line-transect surveys and whale-watching records. In a simulation with one month of survey data and twelve months of opportunistic data, the integrated model recovered spatiotemporal distribution patterns well (median correlation with the true pattern = 0.91) and estimated monthly abundance with a mean error of +10.7%, outperforming single-source models. In a case study of common dolphins (Delphinus delphis) off mainland Portugal, integration improved the spatial accuracy of predictions, although weak covariate effects limited the temporal variation the model could resolve. These results show that integration adds the most value when the two data sources resolve complementary aspects of distribution, in this case broad spatial structure from the survey and temporal replication from whale-watching, while temporal predictions remain limited when covariates carry weak seasonal signal. The framework is general and can be extended to other taxa, systems, and combinations of structured and opportunistic data by substituting the relevant observation models.

ecology↗

Genetic variance in spider mites reveals trade-offs: lines with higher growth rate suffer stronger competition but exert stronger reproductive interference

O_LIWithin-species individual variation has been gaining increased attention in ecological studies of species interactions. Yet, these studies rarely consider genetic variation and potential genetic correlations among traits. Moreover, traits beyond those associated with trophic interactions are mostly overlooked. Filling these gaps is important to fully understand the relevance of trait variation in both the ecology and evolution of species interactions. C_LIO_LIWe addressed this using inbred lines of Tetranychus cinnabarinus, a spider mite species that often engages in antagonistic interactions with its congeneric T. urticae. Specifically, we measured (a) the intrinsic growth rate and the sex ratio in the absence of food competition and reproductive interference; (b) food competition against a density gradient of con- or heterospecific competitors in absence of reproductive interference; (c) reproductive interference in absence of food competition; and (d) the body size of adult females and males. C_LIO_LIWe found significant genetic variance (i.e., broad-sense heritability) among lines for all variables except for the effect of T. cinnabarinus on its heterospecific competitor via food competition. Moreover, we showed that lines with higher intrinsic growth were more sensitive to intra- and inter-specific competition for food but exerted stronger reproductive interference on heterospecifics. In addition, the higher the proportion of sons produced by a line, the more resilient it was to reproductive interference but also the lower its growth rate. No genetic correlations were found between any variable and body size. C_LIO_LIOur results indicate that considering the genetic correlations among traits involved in both trophic and sexual interactions is key to understanding the role of individual variation in species interactions and their evolution. C_LI

evolutionary biology↗

The association of Mediterranean plant species with herbivorous arthropods and its effect on pest abundance in organic vineyards

Non-crop plant resources, such as hedgerows and adjacent woodland areas, may impact the distribution of pest species in the crop. Knowledge on the associations between plants and arthropods as well as their impact on pest distribution is thus key to adequately manage agroecosystems. We selected a number of native Mediterranean plant species located around organic vineyards in Southern Portugal and determined their associations with species of Auchenorrhyncha and phytophagous tetranychid and tenuipalpid mites, including the main species of vineyard pests in the area. We also tested if the abundance of vineyard pests is affected by the distance to the edge and the species of plants present. Most non-crop plants and ground cover vegetation harbored very low numbers of leafhopper pests. Rubus ulmifolius and Tamarix africana proved to be a repository of non-pest Auchenorrhyncha species, with the former also serving as winter repository of the pest Jacobiasca lybica. Rosa canina and Fraxinus angustifolia hosted abundant populations of the spider mite Tetranychus urticae. Still, plots next to plant biodiverse margins harbored fewer numbers of T. urticae, when compared with plots next to other vineyards. Furthermore, pest abundance in vineyards increased with growing distance to plant biodiverse margins. Our results high-light the benefits of biodiverse margins in reducing pest abundance and point to the importance of a good selection of plant species when managing and planning these non-crop plant resources.

ecology↗

Wolbachia strengthens the match between pre-mating and early post-mating isolation in spider mites

Endosymbiotic reproductive manipulators are widely studied as sources of post-zygotic isolation in arthropods, but their effect on pre-zygotic isolation between genetically differentiated populations has garnered less attention. We tested this using two partially isolated populations of the red and green colour forms of Tetranychus urticae, either uninfected or infected with different Wolbachia strains, one inducing cytoplasmic incompatibility and the other not. We first investigated male and female preferences, and found that, in absence of infection, females were not choosy but all males preferred red-form females. Wolbachia effects were more subtle, with only the CI-inducing strain slightly strengthening colour-form based preferences. We then performed a double-mating experiment to test how incompatible matings affect subsequent mating behaviour and offspring production, as compared to compatible matings. Females mated with an incompatible male (infected and/or heterotypic) were more attractive and/or receptive to subsequent (compatible) matings, although analyses of offspring production revealed no clear benefit for this re-mating behaviour (i.e., apparently unaltered first male sperm precedence). Finally, by computing the relative contributions of each reproductive barrier to total isolation, we showed that pre-mating isolation matches both host-associated and Wolbachia-induced post-mating isolation, suggesting that Wolbachia could contribute to reproductive isolation in this system.

evolutionary biology↗

Intraspecific density changes the impact of interspecific competitors on parasite infection traits in multiple infections

Co-infections are frequent, with consequences for parasite life-history traits expressed at within- and between-host levels. However, little is known about whether the effect of interspecific competitors on traits are correlated or independent or if they change with intraspecific competition. To address this, we investigated the occurrence of genetic correlations among within- and betweenhost traits at different intra-specific densities of inbred lines of the spider mite, Tetranychus urticae with its competitor T. evansi. First, we found T. evansi presence on a shared host leaf produced a negative (non-genetic) correlation between virulence (leaf damage) and number of daughters (transmitting stages) at intermediate intraspecific densities; this same relationship was not significant without competitors. Second, we show interspecific competitors increases transmission to adjacent leaf discs, measured as movement of adult T. urticae females, but only at low and intermediate intraspecific densities. Finally we tested whether within-host traits (virulence and transmitting stages) were correlated with between-host traits (movement to adjacent patches), with or without competitors, at different conspecific densities. We found traits were mostly independent; interspecific competitors may increase transmission across hosts without affecting virulence (or vice versa). These independent effects on within- and between-host traits indicate competition may impact epidemiology and parasite trait evolution.

evolutionary biology↗

Sex in the kitchen: non-additive effects of competition for food and reproductive interference on coexistence outcomes between closely related species.

Competition for food and reproductive interference (negative interspecific sexual interactions) have been identified as major drivers of species exclusion. Still, how these biotic interactions jointly determine competitive dominance remains largely unknown. We tackle this by coupling population models and laboratory experiments with two sibling species of spider mites. Using experiments specifically designed to measure the single and combined effects of food competition and reproductive interference, we first show that the strength and symmetry of reproductive interference between species changes in presence of food competition. Next, we show that population models incorporating each type of interaction alone lead to markedly different predictions, from exclusion of the inferior competitor for food, to priority effects instead favouring the latter under the sole effect of reproductive interference. Moreover, accounting for the observed reduction in the strength of reproductive interference in the presence of food competition changes the threshold frequency determining the dominant competitor when both interactions are at play, from equal chances for the two species to exclude the other depending on their initial frequency, to favouring the superior competitor for food except when it is extremely rare. Finally, we showed that the model generates accurate predictions for population dynamics in an independent population cage experiment, indicating that our approach captures the most relevant processes governing the outcome of interactions between competing spider mite species. Altogether, our results suggest that trophic interactions can modulate sexual interactions, significantly impacting population dynamics and competitive outcomes. Hence, the joint consideration of food competition and reproductive interference is critical to accurately predict and understand species coexistence.

ecology↗

Spider mites collectively avoid plants with cadmium irrespective of their frequency or the presence of competitors

Accumulation of heavy metals by plants can serve as a defence against herbivory. Herbivores, in turn, may avoid feeding on contaminated tissues. Such avoidance, however, may hinge upon the specific conditions faced by herbivores. Here, we tested whether the spider mite Tetranychus urticae avoids tomato plants contaminated with cadmium in presence of conspecifics or heterospecifics and depending on the frequency of contaminated plants. We show that individual spider mite females do not preferentially move to leaf tissues with or without cadmium, despite clear costs on their performance. However, in a set-up where 200 mites were simultaneously given the choice between four plants with or without cadmium, they collectively avoided plants with cadmium, irrespective of the proportion of plants with cadmium. In addition, T. urticae did not discriminate between plants infested with its competitor T. evansi and other uncontaminated plants but they preferred plants with competitors when the other plants contained cadmium. Our results show that aggregation may facilitate avoidance of contaminated plants. They also indicate that cadmium accumulation in plants is a stronger selective pressure than interspecific competition with T. evansi. Therefore, collective avoidance of metal-accumulating plants by herbivores is robust to environmental conditions and may have important consequences for species distribution and interactions in metal contaminated sites.

ecology↗

Evolution in abiotic environments shapes coexistence between two spider mite species

Adaptation to abiotic stresses generally relies on traits that are not independent from those affecting species interactions. Still, the impact of such evolutionary processes on coexistence remains elusive. Here, we studied two spider mite species evolving separately on tomato plants that hyper-accumulated cadmium, a stressful environment for herbivores, or on plants without cadmium. Through experimental evolution and structural stability theory, we found that both species coexist in the cadmium environment, but evolution of a single species in cadmium leads to exclusion. However, when both species evolve in cadmium they can coexist. This shift occured due to a simultaneous increase in intra and a decrease in interspecific competition in that environment. These predictions were further confirmed with complementary experiments of population dynamics. Therefore, population shifts to novel environments, even in absence of interspecific competitors, may have unforeseen evolutionary consequences for community composition and the maintenance of species diversity.

evolutionary biology↗

Shaken, not shifted: Genotypic variation tunes how interspecific competition shapes niches

Individual variation in resource use as well as in the response to competitors has been recognized as playing an important role is species interactions. Still, we have as yet little information on whether such responses have a genetic basis as well as on how they affect each other. Here, we tested whether 20 genetically inbred lines of the spider mite Tetranychus evansi vary in their response to a gradient of cadmium concentration within plants as well as in their propensity to reshape niches when facing interspecific competition along this gradient. In absence of interspecific competitors, most lines were negatively affected by cadmium, albeit often in a non-linear fashion. Morevoer, half of the lines exhibited changes in the curvature of the relationship between number of females and cadmium concentration when facing competition with the congeneric T. urticae. Inbred lines also showed a shallower decay in offspring number along the cadmium gradient in presence of interspecific competition. Our findings provide evidence for large, partly genetic, variation in resource use and in the response to interspecific competition in heterogeneous environments. Moreover, we show that genotype responses to interspecific competition is contingent upon their response to an environmental gradient. Together, our results thus emphasize the importance of considering intraspecific variation in responses to interspecific competition, providing novel insights to link intra- and interspecific levels of biodiversity.

ecology↗

Limits to the adaptation of herbivorous spider mites to metal accumulation in homogeneous and heterogeneous environments

Metal accumulation is used by some plants as a defence against herbivores. Yet, herbivores may adapt to these defences, becoming less susceptible. Moreover, ecosystems often contain plants that do and do not accumulate metals, and such heterogeneity may affect herbivore adaptation. Surprisingly, few studies have tested this. Tomato plants accumulate cadmium, affecting the performance of the herbivorous spider mite Tetranychus evansi. Here, we performed experimental evolution to test whether these mites adapt to plants with high cadmium concentrations, in homogeneous (plants with cadmium) or heterogeneous (plants with and without cadmium) environments. We measured fecundity, hatching rate and the number of adult offspring after 12 and 33 generations and habitat choice after 14 and 51 generations, detecting no trait change, which implies absence of adaptation. We then tested whether this absence of adaptation was due to a lack of genetic variation in the traits measured and, indeed, additive genetic variance was low for the measured traits. Possibly, we did not measure the traits that contributed to population persistence on plants with cadmium. Interestingly, despite no signs of adaptation we observed a decrease in fecundity and number of adult offspring produced in cadmium-free plants, in the populations evolving in environments with cadmium. Being this the case, evolving in environments with cadmium may reduce the growth rate of spider mite populations on non-accumulating plants as well. Nevertheless, adaptation to metal accumulation may occur via herbivore traits not commonly measured, which calls for broader studies on this topic.

evolutionary biology↗

Context-dependent effects of temperature and community complexity on trophic interaction strength in a mite community

Both temperature and community complexity are known to affect trophic interaction strength (TIS), but whether their effect is additive or not is as yet an open question. Here we used a 2-predator/3-prey system consistently occurring in avocado orchards to explore the effects of increasing warming and community complexity on the strength of predator:prey trophic interactions. The two predator species differed in their diet breath (a carnivore and an omnivore) and the prey types included a herbivore, heterospecific juvenile predators, and/or pollen. Overall, analyses revealed multiplicative effects of community complexity and both temperature and predator diet breath on the net predator:prey(s) TIS. Indeed, warming led to increased TIS in the community with omnivore as top predator, but only in absence of its preferred food source. When the carnivore was the top predator, in contrast, higher temperatures led to TIS being more negative, but only for the IGprey. We conclude that sources of context dependence in specific systems need to be identified to unveil effects of warming on communities.

ecology↗

Trait-specific indirect effects underlie variation in the response of spiders to cannibalistic social partners

Organisms may respond in different ways to the risk posed by conspecifics, but the cause of such variation remains elusive. Here, we use a half-sib/full-sib design to evaluate the contribution of (indirect) genetic or environmental effects to the behavioral response of the cannibalistic wolf spider Lycosa fasciiventris (Dufour, 1835) towards conspecific cues. Spiders showed variation in relative occupancy time, activity, and velocity on patches with or without conspecific cues, but direct genetic variance was only found for occupancy time. These three traits were correlated and could be lumped in a principal component: spiders spending more time in patches with conspecific cues moved less and at a lower rate in those areas. Genetic and/or environmental components of carapace width and weight loss in the social partner were significantly correlated with the principal component of focal individuals. Variation in these traits may reflect the quality and/or quantity of cues produced by social partners, hence focal individuals were likely behaving along a continuum of strategies in response to the risk posed by social partners. Therefore, environmental and genetic trait variation in the social partners may be key to maintain trait diversity in focal individuals, even in the absence of direct genetic variation.

evolutionary biology↗

Multiple mating rescues offspring sex ratio but not productivity in a haplodiploid exposed to developmental heat stress

O_LIReproduction is generally more sensitive to high temperatures than survival and arguably a better predictor of the response of populations to climate change than survival estimates. Still, how temperature simultaneously impacts male and female reproductive success, the mating system and the operational sex ratio remains an open question. C_LIO_LIHere, we addressed how a sublethal high temperature affects the reproductive system of the haplodiploid spider mite Tetranychus urticae. Males and females maintained at 25{degrees}C or 36{degrees}C during development were paired and the fertility of both sexes, their mating and remating eagerness, and the paternity of the offspring of females with different mating histories were measured. C_LIO_LIFemale and male fertility decreased at 36{degrees}C compared to 25{degrees}C, resulting in lower offspring production and a more male-biased sex ratio, respectively, because of haplodiploidy. However, when females remated, the pattern of first male sperm precedence typically seen in this species was disrupted, with more than one male contributing to the offspring. This was accompanied by reduced mating eagerness in pairs with partially sterile males and increased remating eagerness in pairs in which at least one sex was partially sterile in the first mating. C_LIO_LIThe observed temperature-induced changes in pre- and post-copulatory traits allowed restoring the offspring sex ratio but did not lead to the recovery of offspring number. C_LIO_LIOur results show that temperature induces changes in the spider mite mating behaviour and mating system, with potential impact on sexual selection and sexual conflict. However, such changes may not be sufficient to buffer the impact of extreme temperatures on their populations. C_LI

evolutionary biology↗

Virulence constrains transmission even in the absence of a genetic trade-off

The virulence-transmission trade-off predicts that parasite fitness peaks at intermediate virulence. However, whether this relationship is driven by the environment or genetically determined and if it depends on transmission opportunities remains unclear. We tackled these issues using inbred lines of the macro-parasitic spider-mite Tetranychus urticae. When transmission was not possible during the infection period, we observed a hump-shaped relationship between virulence and parasite fitness, as predicted by theory. This was environmentally driven, as no genetic correlation between traits was detected. However, when transmission to uninfected hosts occurred during the infection period, virulence was positively, environmentally and genetically correlated with parasite fitness. Therefore, the virulence-transmission trade-off depends on within-host dynamics and on the timing of transmission, rather than on a genetic correlation. This fundamental correlation may thus be easier to manipulate than previously thought.

evolutionary biology↗

Order of arrival promotes coexistence via spatial niche preemption by the weak competitor

Historical contingency, such as the order of species arrival, can modify competitive outcomes via niche modification or preemption. However, how these mechanisms ultimately modify stabilising niche and average fitness differences remains largely unknown. By experimentally assembling two congeneric spider mite species feeding on tomato plants during two generations, we show that order of arrival affects species competitive ability and changes the outcome of competition. Contrary to expectations, order of arrival did not cause positive frequency dependent priority effects. Instead, coexistence was predicted when the inferior competitor (Tetranychus urticae) arrived first. In that case, T. urticae colonised the preferred feeding stratum (leaves) of T. evansi leading to spatial niche preemption, which equalised fitness and reduced niche differences, driving community assembly to a close-to-neutrality scenario. Our study demonstrates how the order of species arrival and the spatial context of competitive interactions can jointly determine whether species can coexist.

ecology↗

Wolbachia and host intrinsic reproductive barriers contribute additively to post-mating isolation in spider mites

AO_SCPLOWBSTRACTC_SCPLOWWolbachia are widespread maternally-inherited bacteria suggested to play a role in arthropod host speciation through induction of cytoplasmic incompatibility, but this hypothesis remains controversial. Most studies addressing Wolbachia-induced incompatibilities concern closely-related populations, which are intrinsically compatible. Here, we used three populations of two genetically differentiated colour forms of the haplodiploid spider mite Tetranychus urticae to dissect the interaction between Wolbachia-induced and host-associated incompatibilities, and to assess their relative contribution to post-mating isolation. We found that these two sources of incompatibility act through different mechanisms in an additive fashion. Host-associated incompatibility contributes 1.5 times more than Wolbachia-induced incompatibility in reducing hybrid production, the former through an overproduction of haploid sons at the expense of diploid daugters (ca. 75% decrease) and the latter by increasing the embryonic mortality of daughters (by ca. 49%). Furthermore, regardless of cross direction, we observed near-complete F1 hybrid sterility and complete F2 hybrid breakdown between populations of the two forms, but that Wolbachia did not contribute to this outcome. This study identifies the mechanistic independence and additive nature of host-intrinsic and Wolbachia-induced sources of isolation. It suggests that Wolbachia could drive reproductive isolation in this system, thereby potentially affecting host differentiation and distribution in the field.

evolutionary biology↗

Consequences of population structure for sex allocation and sexual conflict

Both sex allocation and sexual conflict can be modulated by spatial structure. However, how the interplay between the type of dispersal and the scale of competition simultaneously affects these traits in sub-divided populations is rarely considered. We investigated sex allocation and sexual conflict evolution in meta-populations of the spider mite Tetranychus urticae evolving under budding (pairing females from the same patch) or random (pairing females from different patches) dispersal and either local (fixed sampling from each subpopulation) versus global (sampling as a function of subpopulation productivity) competition. Females evolving under budding dispersal produced less female-biased offspring sex ratios than those from the random dispersal selection regimes, contradicting theoretical predictions. In turn, the scale of competition did not have a strong effect on sex allocation. Males evolved under budding dispersal induced less female harm than those exposed to random dispersal, but there was no reduction in female fitness following exposure to multiple mates from either selection regime. This work highlights that population structure can impact the evolution of sex allocation and sexual conflict. We also discuss how selection on either trait may reciprocally affect the evolution of the other, for example via effects on fecundity.

evolutionary biology↗