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Rodrigues, L. R.

Publications and source records attributed to Rodrigues, L. R..

14 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↗

Inducible tomato defences persist in detached leaves, despite differential plant variety and gene-dependent expression

Herbivore and pathogen attacks often lead to the induction of plant defences. Given the intricate nature of such responses, plant integrity is assumed to be a pre-requisite for the successful mounting of defences, a hypothesis supported by work done in plant-pathogen interactions. However, the relevance of plant integrity in plant-herbivore interactions, particularly in direct plant defences, is unclear and lacks empirical molecular validation. To test this, we measured the expression of plant defence-related genes (PPO-D and PI-IIc, involved in the jasmonate signal pathway and PR-1a, involved in the salicylic acid signal pathway) in intact plants and detached leaves of two tomato varieties infested or not with the herbivorous spider mite Tetranychus urticae. We also tested whether defences persisted in detached leaves after one, four, seven or fourteen days of infestation. We found that tomato defences were induced in both intact plants and detached leaves and that the expression of all three genes in detached leaves increased over time, being the increment higher in the two late-expression genes, PI-IIc and PR-1a. Such results suggests that both intact plants and detached leaves can be used in studies addressing herbivore interactions with plant defences. However, induction levels in intact plants and detached leaves varied with plant variety and the gene assessed, ranging from higher expression in detached leaves than in intact plants to the reverse. Hence, studies aiming at identifying the role of specific genes should account for the differential, variety-dependent, role of plant integrity in their expression.

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↗

De novo production of prenylnaringenin compounds by a metabolically engineered Escherichia coli

Prenylnaringenin (PN) compounds, namely 8-prenylnaringenin (8-PN), 3-prenylnaringenin (3-PN), and 6-prenylnaringenin (6-PN), are reported to have several interesting bioactivities. This study aimed to validate a biosynthetic pathway for de novo production of PN in Escherichia coli. A previously optimized E. coli chassis capable of efficiently de novo producing naringenin was used to evaluate eleven prenyltransferases (PTs) for the production of PN compounds. As PT reaction requires dimethylallyl pyrophosphate (DMAPP) as extended substrate that has limited availability inside the cells, clustered regularly interspaced short palindromic repeats (CRISPR) and CRISPR-associated protein 12a (Cas12a) (CRISPR-Cas12a) was used to construct ten boosted DMAPP-E. coli strains. All the PTs, in combination with the naringenin biosynthetic pathway, were tested in these strains. Experiments in 96-well deep well plates identified twelve strains capable of producing PN. E. coli M-PAR-121 with the integration of the 1-deoxy-D-xylulose-5-phosphate synthase (DXS) gene from E. coli (EcDXS) into the lacZ locus of the genome (E. coli M-PAR-121:EcDXS) expressing the soluble aromatic PT from Streptomyces roseochromogenes (CloQ) and the naringenin biosynthetic pathway was selected as the best producer strain. After optimizing the production media in shake flasks, 160.57 {micro}M of 3-PN, 4.4 {micro}M of 6-PN, and 2.66 {micro}M of 8-PN were obtained. The production was then evaluated at the bioreactor scale and 397.57 {micro}M of 3-PN (135.33 mg/L) and 25.61 {micro}M of 6-PN (8.72 mg/L) were obtained. To the best of our knowledge, this work represents the first report of de novo production of PN compounds using E. coli as a chassis.

synthetic 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↗

Monandrous flies do remate: plastic and evolutionary consequences of heat exposure on mating behaviour and fertility in Drosophila subobscura

Recent work has reinforced the importance of fertility in predicting population persistence under global warming, especially male fertility. However, most studies on mating and reproductive performance have used as model organism polyandrous species, remaining unclear if and how will monandrous species respond. This is unfortunate as one could expect monandrous species to be particularly susceptible, given their inability to use sperm from multiple males to prevent reduced progeny production due to male sterility. It could be that monandrous females can overcome this toll in fertility by plastically changing their mating rate, or that monandrous populations evolve the ability to remate upon repeated exposure to heat. To test this, we studied the real-time evolution as well as the thermal plastic response of two geographically distinct populations of the monandrous species Drosophila subobscura after 45 generations evolving under a warming scenario. We assessed the impact of heat on male mating behaviour and fertility, as well as the impact of reduced male fertility on female mating behaviour and fertility. We found that in males the toll in mating behaviour due to heat can be recovered with time, whereas that in reproductive success cannot. On the other hand, females exposed to heat-stressed males significantly increased their remating rate, allowing to recover considerably their own reproductive success. Interestingly, most responses were plastic, with no striking effect of adaptation to warming nor of geographical origin. Our work brings new insights into the effects of heat on monandrous species and establishes a model to study how a shift in mating system may affect species ability to respond to climate change.

evolutionary biology↗

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↗

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↗

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↗

Creating outbred and inbred populations of haplodiploid mites to measure adaptive responses in the lab

Laboratory studies are often criticized for not being representative of processes occurring in natural populations. This can be partially mitigated by using lab populations that capture large amounts of variation. Additionally, many studies addressing adaptation of organisms to their environment are done with laboratory populations, using quantitative genetics or experimental evolution methodologies. Such studies rely on populations that are either highly outbred or inbred. However, the methodology underlying the generation of such biological resources are usually not explicitly documented. Given their small size, short generation time, amenability to laboratory experimentation and knowledge of their ecological interactions, haplodiploid spider mites are becoming a widely used model organism. Here, we describe the creation of outbred populations of two species of spider mites, Tetranychus urticae and T. evansi, obtained by performing controlled crosses between individuals from field-collected populations. Subsequently, from the outbred population of T. evansi, we derived inbred lines, by performing several generations of sib-mating. These can be used to measure broad-sense heritability as well as correlations among traits. Finally, we outline an experimental evolution protocol that can be widely used in other systems. Sharing these biological resources with other laboratories and combining them with the available powerful genetic tools for T. urticae (and other species) will allow consistent and comparable studies that greatly contribute to our understanding of ecological and evolutionary processes.

evolutionary biology↗

Environments with a high probability of incompatible crosses do not select for mate avoidance in spider mites

Arthropods are often infected with Wolbachia inducing cytoplasmic incompatibility (CI), whereby crosses between uninfected females and infected males yield unviable fertilized offspring. Although uninfected females benefit from avoiding mating with Wolbachia-infected males, this behaviour is not present in all host species. Here we measured the prevalence of this behaviour across populations of the spider mite Tetranychus urticae. Females from five populations originally fully infected with Wolbachia showed no preference, possibly because they did not face the choice between compatible and incompatible mates in their environment. Hence, to determine whether this behaviour could be selected in populations with intermediate Wolbachia infection frequency, we performed 15 generations of experimental evolution of spider-mite populations under i) full Wolbachia infection, ii) no infection, or iii) mixed infection. In the latter selection regime, where uninfected females were exposed to infected and uninfected males at every generation, mating duration increased relative to the uninfected regime, suggesting the presence of genetic variation for mating traits. However, mate choice did not evolve. Together, these results show that CI-inducing Wolbachia alone does not necessarily lead to the evolution of pre-copulatory strategies in uninfected hosts, even at intermediate infection frequency.

evolutionary biology↗

Costs and benefits of mating with fertilized females in a species with first male sperm precedence

Different patterns of sperm precedence are expected to result in specific mating costs and benefits for each sex, generating different selection pressures on males and females. However, most studies concern species with mixed paternity or last male sperm precedence, neglecting species with first male sperm precedence, in which only the first mating is effective.\n\nHere, we measured costs and benefits of multiple mating for both sexes of the spider mite Tetranychus urticae. First, we assessed the stability of the sperm precedence pattern, by mating females to one, two or several males, immediately after the first mating or 24 hours later. We found complete first male precedence, independently of the mating interval and the number of matings. Females paid a cost of polyandry, as multiply-mated females laid fewer eggs than once-mated females. However, while first males had reduced survival when exposed to an intermediate number of virgin females, second males paid no additional costs by matings with several mated females. Moreover, by mating multiply with mated females, males decreased the total number of offspring sired by first males, which suggests that these matings may entail a relative benefit for second males, despite being ineffective.\n\nOur results show that complex costs and benefits may arise in males in species with first male precedence. How these costs and benefits affect the maintenance of selection for polyandry remains an open question.

evolutionary biology↗

Despite reproductive interference, the net outcome of reproductive interactions among spider mite species is not necessarily costly

This preprint has been reviewed and recommended by Peer Community in Evolutionary Biology (http://dx.doi.org/10.24072/pci.evolbiol.100025). Reproductive interference is considered a strong ecological force, potentially leading to species exclusion. This supposes that the net effect of reproductive interactions is strongly negative for one of the species involved. Testing this requires a comprehensive analysis of interspecific reproductive interactions, accounting for the order and timing of mating events, and for their effects on either fertility or fecundity. To this aim, we measured reproductive interactions between a focal species, Tetranychus urticae, and an invasive (T.evansi) and a resident (T. ludeni) species, varying the mating sequence and interval, and measuring the effect of such crosses on fecundity and offspring sex ratio (a measure of fertility, as these species are haplodiploid). We found that mating with heterospecifics affected fecundity and sex ratio negatively, but also positively, depending on the species involved, and on the order and timing of mating events. Overall, the net effect of reproductive interactions was weak despite strong effects of particular events. In natural situations, the outcome of reproductive interactions will thus hinge upon the frequency of each event.

ecology↗