Search bioRxiv⌕ Search

Biology subjects

Olazcuaga, L.

Publications and source records attributed to Olazcuaga, L..

12 recordsLinked to original sources

Warming and predation drive rapid evolution of ecosystem functioning but not functional traits

Global environmental change can rapidly reshape phenotypic trait distributions through adaptive and neutral processes. Yet, disentangling their relative contributions remains a major challenge, particularly for traits underpinning ecosystem functioning. Using a two-year mesocosm study, we experimentally evolved Asellus aquaticus under contrasting temperature and predation regimes to test how the joint influence of these global change pressures shape the evolution of traits and ecosystem functioning. We show that classic functional traits (body size and metabolic rate) showed no evidence of divergent evolution across evolutionary conditions, while ecosystem function itself, namely decomposition rate, has evolved rapidly and differently depending on evolutionary conditions, with the highest decomposition rate observed for Asellus populations exposed to high temperatures in the absence of their predator. A Pst/Fst comparison revealed that divergence in metabolic rate among evolutionary conditions was mainly driven by genetic drift, whereas, for body mass and decomposition rate, non-neutral processes (natural selection and/or plasticity) were also involved, albeit in a different way. By demonstrating that predation and temperature can influence the evolution of an ecosystem function over a few generations, this study represents an important first step toward uncovering the combined effects of global change on the eco-evolutionary dynamics of ecosystems.

evolutionary biology↗

Density dependence impedes evolutionary rescue

Evolutionary rescue allows populations to adapt and persist despite severe environmental change. While well studied under density-independent conditions, the role of density dependence, including competition, remains unclear. Theoretical models offer conflicting predictions, with density dependence either increasing extinction risk or enhancing adaptation. We empirically tested how density dependence influences evolutionary rescue by exposing experimental populations to a stressful environment for six generations under density-dependent or independent conditions, with populations where either evolution was possible or was prevented by replacing individuals each generation. Density dependence suppressed population size and increased extinction risk, whereas density independence enabled rapid growth, especially in genetically diverse populations where evolution was possible. Although density dependence raises extinction risk, it does not prevent populations from responding to selection, since surviving density-dependent populations still exhibited increased intrinsic and realized fitness. These findings reconcile theoretical discrepancies, showing density dependence can simultaneously increase extinction risk but may favor adaptation. Our results underscore the importance of considering density dependence in conservation strategies.

evolutionary biology↗

Immigration delays but does not prevent adaptation following environmental change: experimental evidence

In todays rapidly changing world, it is critical to examine how animal populations will respond to severe environmental change. Following events such as pollution or deforestation that cause populations to decline, extinction will occur unless populations can adapt in response to natural selection, a process called evolutionary rescue. Theory predicts that immigration can delay extinction and provide novel genetic material that can prevent inbreeding depression and facilitate adaptation. However, when potential source populations have not experienced the new environment before (i.e., are naive), immigration can counteract selection and constrain adaptation. This study evaluated the effects of immigration of naive individuals on evolutionary rescue using the red flour beetle, Tribolium castaneum, as a model system. Small populations were exposed to a challenging environment, and three immigration rates (zero, one, or five migrants per generation) were implemented with migrants from a benign environment. Following an initial decline in population size across all treatments, populations receiving no immigration gained a higher growth rate one generation earlier than those with immigration, illustrating the constraining effects of immigration on adaptation. After seven generations, a reciprocal transplant experiment found evidence for adaptation regardless of immigration rate. Thus, while the immigration of naive individuals briefly delayed adaptation, it did not increase extinction risk or prevent adaptation following environmental change.

evolutionary biology↗

Population demographic history and evolutionary rescue: influence of a bottleneck event

Rapid environmental change presents a significant challenge to the persistence of natural populations. Rapid adaptation that increases population growth, enabling populations that declined following severe environmental change to grow and avoid extinction, is called evolutionary rescue. Numerous studies have shown that evolutionary rescue can indeed prevent extinction. Here, we extend those results by considering the demographic history of populations. To evaluate how demographic history influences evolutionary rescue, we created 80 populations of red flour beetle, Tribolium castaneum, with three classes of demographic history: diverse populations that did not experience a bottleneck, and populations that experienced either an intermediate or a strong bottleneck. We subjected these populations to a new and challenging environment for six discrete generations and tracked extinction and population size. Populations that did not experience a bottleneck in their demographic history avoided extinction entirely, while more than 20% of populations that experienced an intermediate or strong bottleneck went extinct. Similarly, among the extant populations at the end of the experiment, adaptation increased the growth rate in the novel environment the most for populations that had not experienced a bottleneck in their history. Taken together, these results highlight the importance of considering the demographic history of populations to make useful and effective conservation decisions and management strategies for populations experiencing environmental change that pushes them toward extinction.

evolutionary biology↗

How density dependence, genetic erosion, and the extinction vortex impact evolutionary rescue

Following severe environmental change that reduces mean population fitness below replacement, populations must adapt to avoid eventual extinction, a process called evolutionary rescue. Models of evolutionary rescue demonstrate that initial size, genetic variation, and degree of maladaptation influence population fates. However, many models feature populations that grow without negative density dependence or with constant genetic diversity despite precipitous population decline, assumptions likely to be violated in conservation settings. We examined the simultaneous influences of density-dependent growth and erosion of genetic diversity on populations adapting to novel environmental change using stochastic, individual-based simulations. Density dependence decreased the probability of rescue and increased the probability of extinction, especially in large and initially well-adapted populations that previously have been predicted to be at low risk. Increased extinction occurred shortly following environmental change, as populations under density dependence experienced more rapid decline and reached smaller sizes. Populations that experienced evolutionary rescue lost genetic diversity through drift and adaptation, particularly under density dependence. Populations that declined to extinction entered an extinction vortex, where small size increased drift, loss of genetic diversity, and the fixation of maladaptive alleles, hindered adaptation, and kept populations at small densities where they were vulnerable to extinction via demographic stochasticity.

ecology↗

Metabolic consequences of various fruit-based diets in a generalist insect species

Most phytophagous insect species exhibit a limited diet breadth and specialize on few or a single host plant. In contrast, some species display a remarkably large diet breadth, with host plants spanning several families and many species. It is unclear, however, whether this phylogenetic generalism is supported by a generic metabolic use of common host chemical compounds ( metabolic generalism) or alternatively by distinct uses of diet-specific compounds ( multi-host metabolic specialism)? Here, we simultaneously investigated the metabolomes of fruit diets and of individuals of a generalist phytophagous species, Drosophila suzukii, that developed on them. The direct comparison of metabolomes of diets and consumers enabled us to disentangle the metabolic fate of common and rarer dietary compounds. We showed that the consumption of biochemically dissimilar diets resulted in a canalized, generic response from generalist individuals, consistent with the metabolic generalism hypothesis. We also showed that many diet-specific metabolites, such as related to the particular color, odor or taste of diets, were not metabolized, and rather accumulated in consumer individuals, even when probably detrimental to fitness. As a result, while individuals were mostly similar across diets, the detection of their particular diet was straightforward. Our study thus supports the view that dietary generalism may emerge from a passive, opportunistic use of various resources, contrary to more widespread views of an active role of adaptation in this process. Such a passive stance towards dietary chemicals, probably costly in the short term, might favor the later evolution of new diet specializations.

ecology↗

Fruit phosphorus concentration does not affect oviposition preference in the invasive pest Drosophila suzukii

The broad variation in host use among polyphagous insects is well documented but still poorly understood. In numerous pest insects, the proximate mechanisms responsible for variation in oviposition preference among host plants remain to be elucidated. The invasive crop pest, Drosophila suzukii, attacks a wide range of host fruits. Females prefer ovipositing on particular fruit media (blackberry, cherry, blackcurrant) that are rich in phosphorus. As phosphorus is known to be involved in female reproduction in insect species such as Drosophila, it could drive oviposition preference in D. suzukii. Phosphorus is either present as inorganic or organic phosphate in fruits. As the absolute content in macromolecules associated with phosphate in fruits (i.e. proteins and carbohydrates) do not affect oviposition in D. suzukii, we tested for the effect of inorganic phosphate on oviposition preference. We measured the egg-laying preferences of D. suzukii in a choice environment containing 12 artificial media with increasing content in inorganic phosphate (monopotassium dihydrogen phosphate). In our assay, D. suzukii females did not prefer ovipositing in media with high inorganic phosphate content compared to media with lower inorganic phosphate content. As a confirmation, we verified the previous result of a higher female preference for media made of phosphorus-rich fruits (blackberry, cherry, blackcurrant). The higher preference for phosphorus-rich fruits could be driven by macromolecules containing phosphorus (e.g. phospholipids) or by the presence of one or more molecules that do not contain phosphorus, but that happen to be correlated to fruit phosphorus content. Studying the proximate mechanisms driving host use will ultimately help improve the management of D. suzukii and other crop pests.

ecology↗

Rapid and transient evolution of local adaptation to seasonal host fruits in an invasive fly

Both local adaptation and adaptive phenotypic plasticity can influence the match between phenotypic traits and local environmental conditions. Theory predicts that environments stable for multiple generations promote local adaptation, while highly heterogeneous environments favor adaptive phenotypic plasticity. However, when environments have periods of stability mixed with heterogeneity, the relative importance of local adaptation and adaptive phenotypic plasticity is unclear. Here, we used Drosophila suzukii as a model system to evaluate the relative influence of genetic and plastic effects on the match of populations to environments with periods of stability from three to four generations. This invasive pest insect can develop within different fruits, and persists throughout the year in a given location on a succession of distinct host fruits, each one being available for only a few generations. Using reciprocal common environment experiments of natural D. suzukii populations collected from cherry, strawberry and blackberry, we found that both oviposition preference and offspring performance were higher on medium made with the fruit from which the population originated, than on media made with alternative fruits. This pattern, which remained after two generations in the laboratory, was analyzed using a statistical method we developed to quantify the contributions of local adaptation and adaptive plasticity in determining fitness. Altogether, we found that genetic effects (local adaptation) dominate over plastic effects (adaptive phenotypic plasticity). Our study demonstrates that spatially and temporally variable selection does not prevent the rapid evolution of local adaptation in natural populations. The speed and strength of adaptation may be facilitated by several mechanisms including a large effective population size and strong selective pressures imposed by host plants. Impact SummaryNatural populations often exhibit good "fit" to the environment they are in. However, environments change over time and space, and following change, the fit between a population and its environment may be poor. A question of long-standing interest is how do populations track changing environments to maintain fitness? Two main mechanisms are known: (i) genetic shifts in the form of local adaptation, in which traits evolve over time through differences in fitness of individuals harboring different genetic variants, and (ii) plastic shifts, or adaptive phenotypic plasticity, in which traits immediately change in response to environmental change. Adaptation is common when environments change over multiple generations, while plasticity is common when environments change over an individuals lifetime. However, it remains unclear whether plasticity or adaptation is more vital to maintaining fitness when environments change at an intermediate pace. Drosophila suzukii is well-suited to evaluating the relative importance of plasticity and adaptation in response to an intermediate pace of environmental change. This invasive pest species experiences an environment that shifts every 1-4 generations as host fruits change over time and space. Here, we studied natural populations of D. suzukii collected from different hosts. Using reciprocal common environment experiments, we evaluated their fitness on their source and alternative hosts. Drosophila suzukii populations were most fit on their source host, successfully tracking an intermediate pace of environmental change. We developed a statistical method to quantify the contributions of adaptive plasticity and local adaptation in determining fitness. We found that fitness was mainly maintained through local adaptation to each new host in succession. This study highlights that spatially and temporally variable selection does not prevent local adaptation and, on the contrary, illustrates how rapid the adaptive process can be. It also provides a novel statistical tool that can be applied to other systems

evolutionary biology↗

The origin and maintenance of microbial symbionts in Drosophila larvae

Little is known on the origin and maintenance of symbionts associated with Drosophila larvae in natura, which restricts the understanding of Drosophila-extracellular microorganism symbiosis in the light of evolution. Here, we studied the origin and maintenance of symbionts of Drosophila larvae under ecologically realistic conditions, to our knowledge for the first time, using yeast and bacterial isolates and two Drosophila species: the model organism D. melanogaster and the invasive pest D. suzukii. We discovered that Drosophila females and males both transmit yeast and bacteria symbionts to larvae. In addition, several symbiotic yeasts initially associated with larvae were conserved throughout host life cycle and transmitted to offspring. Our results suggest that stable associations of Drosophila flies with bacteria and yeasts may exist in natura and constitute a step forward in the understanding of wild Drosophila-microorganism symbioses.

ecology↗

How do invasion syndromes evolve? An experimental evolution approach using the ladybug Harmonia axyridis

Experiments comparing native to introduced populations or distinct introduced populations to each other show that phenotypic evolution is common and often involves a suit of interacting phenotypic traits. We define such sets of traits that evolve in concert and contribute to the success of invasive populations as an invasion syndrome. The invasive Harlequin ladybird Harmonia axyridis displays such an invasion syndrome with, for instance, females from invasive populations being larger and heavier than individuals from native populations, allocating more resources to reproduction, and spreading reproduction over a longer lifespan. Invasion syndromes could emerge due to selection acting jointly and directly on a multitude of traits, or due to selection on one or a few key traits that drive correlated indirect responses in other traits. Here, we investigated the degree to which the H. axyridis invasion syndrome would emerge in response to artificial selection on either female body mass or on age at first reproduction, two traits involved in their invasion syndrome. To further explore the interaction between environmental context and evolutionary change in molding the phenotypic response, we phenotyped the individuals from the selection experiments in two environments, one with abundant food resources and one with limited resources. The two artificial selection experiments show that the number of traits showing a correlated response depends upon the trait undergoing direct selection. Artificial selection on female body mass resulted in few correlated responses and hence poorly reproduced the invasion syndrome. In contrast, artificial selection on age at first reproduction resulted in more widespread phenotypic changes, which nevertheless corresponded only partly to the invasion syndrome. The artificial selection experiments also revealed a large impact of diet on the traits, with effects dependent on the trait considered and the selection regime. Overall, our results indicate that direct selection on multiple traits was likely necessary in the evolution of the H. axyridis invasion syndrome. Furthermore, they show the strength of using artificial selection to identify the traits that are correlated in different selective contexts, which represents a crucial first step in understanding the evolution of complex phenotypic patterns, including invasion syndromes.

evolutionary biology↗

A whole-genome scan for association with invasion success in the fruit fly Drosophila suzukii using contrasts of allele frequencies corrected for population structure

Evidence is accumulating that evolutionary changes are not only common during biological invasions but may also contribute directly to invasion success. The genomic basis of such changes is still largely unexplored. Yet, understanding the genomic response to invasion may help to predict the conditions under which invasiveness can be enhanced or suppressed. Here we characterized the genome response of the spotted wing drosophila Drosophila suzukii during the worldwide invasion of this pest insect species, by conducting a genome-wide association study to identify genes involved in adaptive processes during invasion. Genomic data from 22 population samples were analyzed to detect genetic variants associated with the status (invasive versus native) of the sampled populations based on a newly developed statistic, we called C2, that contrasts allele frequencies corrected for population structure. This new statistical framework has been implemented in an upgraded version of the program BO_SCPLOWAYC_SCPLOWPO_SCPLOWASSC_SCPLOW. We identified a relatively small set of single nucleotide polymorphisms (SNPs) that show a highly significant association with the invasive status of populations. In particular, two genes RhoGEF64C and cpo, the latter contributing to natural variation in several life-history traits (including diapause) in Drosophila melanogaster, contained SNPs significantly associated with the invasive status in the two separate main invasion routes of D. suzukii. Our methodological approaches can be applied to any other invasive species, and more generally to any evolutionary model for species characterized by non-equilibrium demographic conditions for which binary covariables of interest can be defined at the population level.

evolutionary biology↗

Evolution of trade-offs across environments following experimental evolution of the generalist Drosophila suzukii to different fruit media

The process of local adaptation involves differential changes in fitness over time across different environments. While experimental evolution studies have extensively tested for patterns of local adaptation at a single time point, there is relatively little research that examines fitness more than once during the time course of adaptation. We allowed replicate populations of the fruit pest Drosophila suzukii to evolve in one of eight different fruit media. After five generations, populations with the highest initial levels of maladaptation had mostly gone extinct, whereas experimental populations evolving on cherry, strawberry and cranberry media had survived. We measured the fitness of each surviving population in each of the three fruit media after five and after 26 generations of evolution. After five generations, adaptation to each medium was associated with increased fitness in the two other media. This was also true after 26 generations, except when populations that evolved on cranberry medium developed on cherry medium. These results suggest that, in the theoretical framework of a fitness landscape, the fitness optima of cherry and cranberry media are the furthest apart. Our results show that studying how fitness changes across several environments and across multiple generations provides insights into the dynamics of local adaptation that would not be evident if fitness were analyzed at a single point in time. By allowing a qualitative mapping of an experimental fitness landscape, our approach will improve our understanding of the ecological factors that drive the evolution of local adaptation in D. suzukii.

evolutionary biology↗