Direct and correlated responses to selection in a host-parasite system: testing for the emergence of genotype specificity

Genotype x environment interactions can facilitate coexistence of locally adapted specialists. Interactions evolve if adaptation to one environment trades off with performance in others. We investigated whether evolution on one host genotype traded off with performance on others in long-term experimental populations of different genotypes of the protozoan Paramecium caudatum, infected with the bacterial parasite Holospora undulata. A total of nine parasite selection lines evolving on three host genotypes and the ancestral parasite were tested in a cross-infection experiment. We found that evolved parasites produced more infections than did the ancestral parasites, both on host genotypes they had evolved on (positive direct response to selection) and on genotypes they had not evolved on (positive correlated response to selection). On two host genotypes, a negative relationship between direct and correlated responses indicated pleiotropic costs of adaptation. On the third, a positive relationship suggested cost-free adaptation. Nonetheless, on all three hosts, resident parasites tended to be superior to the average nonresident parasite. Thus genotype specificity (i.e., patterns of local adaptation) may evolve without costs of adaptation, as long as direct responses to selection exceed correlated responses.     

Premating isolation is determined by larval rearing substrates in cactophilic Drosophila mojavensis. IV. Correlated responses in behavioral isolation to artificial selection on a life-history trait

Abstract Studies of behavioral isolation among geographically isolated populations of Drosophila mojavensis have provided an understanding of incipient speciation wherein phylogeny and ecology play a prominent role. Populations of D. mojavensis in mainland Mexico and southern Arizona exhibit low but significant premating isolation from Baja California populations in laboratory mate choice tests. These same populations have undergone considerable life-history evolution in response to use of different host plants, suggesting that behavioral isolation between populations is a pleiotropic consequence of adaptation to different environments, or Mayr's geographic speciation hypothesis. This hypothesis was tested using bidirectional artificial selection on egg-to-adult development time in replicate lines of a mainland and Baja population cultured on two host cacti for 13 generations. Response to selection was greatest in the slow lines cultured on one host, yet there was uneven response in some lines due to variation in cactus tissue quality. Realized heritabilities for development time ranged from 0.04 to 0.16, which is consistent with previous estimates from half-sib/full-sib analyses of genetic variation. In most lines that responded to selection, premating isolation decreased to near zero. Correlated responses in behavioral isolation suggest that adaptation to contrasting environments can cause secondary responses in mate recognition systems that can influence the formation of new species.     

Extent of adaptation is not limited by unpredictability of the environment in laboratory populations of Escherichia coli

Environmental variability is on the rise in different parts of the earth, and the survival of many species depends on how well they cope with these fluctuations. Our current understanding of how organisms adapt to unpredictably fluctuating environments is almost entirely based on studies that investigate fluctuations among different values of a single environmental stressor such as temperature or pH . How would unpredictability affect adaptation when the environment fluctuates between qualitatively very different kinds of stresses? To answer this question, we subjected laboratory populations of Escherichia coli to selection over ~ 260 generations. The populations faced predictable and unpredictable environmental fluctuations across qualitatively different selection environments, namely, salt and acidic pH . We show that predictability of environmental fluctuations does not play a role in determining the extent of adaptation, although the extent of ancestral adaptation to the chosen selection environments is of key importance.     

Do mites evolving in alternating host plants adapt to host switch?

A fluctuating environment may be perceived as a composition of different environments, or as an environment per se, in which it is the fluctuation itself that poses a selection pressure. If so, then organisms may adapt to this alternation. We tested this using experimental populations of spider mites that have been evolving for 45 generations in a homogeneous environment (pepper or tomato plants), or in a heterogeneous environment composed of an alternation of these two plants approximately at each generation. The performance (daily oviposition rate and juvenile survival) of individuals from these populations was tested in each of the homogeneous environments, and in two alternating environments, one every 3 days and the other between generations. To discriminate between potential genetic interactions between alleles conferring adaptation to each host plant and environmental effects of evolving in a fluctuating environment, we compared the performance of all lines with that of a cross between tomato and pepper lines. As a control, two lines within each selection regime were also crossed. We found that crosses between alternating lines and between pepper and tomato lines performed worse than crosses between lines evolving in homogeneous environments when tested in that environment. In contrast, alternating lines performed either better or similarly to lines evolving in homogeneous environments when tested in a fluctuating environment. Our results suggest that fluctuating environments are more than the juxtaposition of two environments. Hence, tests for adaptation of organisms evolving in such environments should be carried out in fluctuating conditions.     

Experimental adaptive radiation in Pseudomonas

We studied the importance of selection and constraint in determining the limits of adaptive radiation and the consequences of adaptive radiation in an experimental system. We propagated four replicate lines of the bacterium Pseudomonas fluorescens derived from a single ancestral clone in 95 environments, where growth was limited by the availability of a single carbon source for 1,000 generations. We then assayed the growth of the ancestral clone and the evolved lines in all 95 environments. Evolved lines increased their performance in almost every selection environment and invaded 70% of the novel environments as a direct response to selection. Direct responses tended to be larger in environments where growth was initially poor. Although evolved lines lost the ability to grow on about three substrates that their ancestor could readily grow on, the correlated response to selection was, on average, positive. The correlated response allowed all of our evolved populations to expand their niches and to occupy collectively the remaining novel habitats. This is inconsistent with classical theories of niche evolution. In the most extreme cases, adaptation occurred through "roundabout selection": lineages became adapted to an environment through selection in another environment but not through selection in the environment itself. Our results indicate that mutation accumulation by neutral drift was responsible for generating the majority of costs of adaptation.     

Evolutionary mismatch along salinity gradients in a Neotropical water strider

The evolution of local adaptation is crucial for the in situ persistence of populations in changing environments. However, selection along broad environmental gradients could render local adaptation difficult, and might even result in maladaptation. We address this issue by quantifying fitness trade‐offs (via common garden experiments) along a salinity gradient in two populations of the Neotropical water strider Telmatometra withei—a species found in both fresh (FW) and brackish (BW) water environments across Panama. We found evidence for local adaptation in the FW population in its home FW environment. However, the BW population showed only partial adaptation to the BW environment, with a high magnitude of maladaptation along naturally occurring salinity gradients. Indeed, its overall fitness was ~60% lower than that of the ancestral FW population in its home environment, highlighting the role of phenotypic plasticity, rather than local adaptation, in high salinity environments. This suggests that populations seemingly persisting in high salinity environments might in fact be maladapted, following drastic changes in salinity. Thus, variable selection imposed by salinization could result in evolutionary mismatch, where the fitness of a population is displaced from its optimal environment. Understanding the fitness consequences of persisting in fluctuating salinity environments is crucial to predict the persistence of populations facing increasing salinization. It will also help develop evolutionarily informed management strategies in the context of global change.     

Mapping the adaptive landscape of a major agricultural pathogen reveals evolutionary constraints across heterogeneous environments

The adaptive potential of pathogens in novel or heterogeneous environments underpins the risk of disease epidemics. Antagonistic pleiotropy or differential resource allocation among life-history traits can constrain pathogen adaptation. However, we lack understanding of how the genetic architecture of individual traits can generate trade-offs. Here, we report a large-scale study based on 145 global strains of the fungal wheat pathogen Zymoseptoria tritici from four continents. We measured 50 life-history traits, including virulence and reproduction on 12 different wheat hosts and growth responses to several abiotic stressors. To elucidate the genetic basis of adaptation, we used genome-wide association mapping coupled with genetic correlation analyses. We show that most traits are governed by polygenic architectures and are highly heritable suggesting that adaptation proceeds mainly through allele frequency shifts at many loci. We identified negative genetic correlations among traits related to host colonization and survival in stressful environments. Such genetic constraints indicate that pleiotropic effects could limit the pathogen’s ability to cause host damage. In contrast, adaptation to abiotic stress factors was likely facilitated by synergistic pleiotropy. Our study illustrates how comprehensive mapping of life-history trait architectures across diverse environments allows to predict evolutionary trajectories of pathogens confronted with environmental perturbations.Subject terms: Population genetics, Plant sciences, Molecular evolution, Fungi     

Thermal adaptation in<Emphasis Type="Italic">Drosophila serrata</Emphasis> under conditions linked to its southern border: Unexpected patterns from laboratory selection suggest limited evolutionary potential

To investigate the ability ofDrosophila serrata to adapt to thermal conditions over winter at the species southern border, replicate lines from three source locations were held as discrete generations over three years at either 19‡C (40 generations) or temperatures fluctuating between 7‡C and 18δC (20 generations). Populations in the fluctuating environment were maintained either with an adult 0‡C cold shock or without a shock. These conditions were expected to result in temperature-specific directional selection for increased viability and productivity under both temperature regimes, and reduced development time under the fluctuating-temperature regime. Selection responses of all lines were tested under both temperature regimes after controlling for carry-over effects by rearing lines in these environments for two generations. When tested in the 19‡C environment, lines evolving at 19‡C showed a faster development time and a lower productivity relative to the other lines, while cold shock reduced development time and productivity of all lines. When tested in the fluctuating environment, productivity of the 7–18‡C lines selected with a cold shock was relatively lower than that of lines selected without a shock, but this pattern was not observed in the other populations. Viability and body size as measured by wing length were not altered by selection or cold shock, although there were consistent effects of source population on wing length. These results provide little evidence for temperature-specific adaptation inD. serrata —although the lines had diverged for some traits, these changes were not consistent with a priori predictions. In particular, there was no evidence for life-history changes reflecting adaptation to winter conditions at the southern border. The potential forD. serrata to adapt to winter conditions may therefore be limited.     

Haploids adapt faster than diploids across a range of environments

Despite a great deal of theoretical attention, we have limited empirical data about how ploidy influences the rate of adaptation. We evolved isogenic haploid and diploid populations of Saccharomyces cerevisiae for 200 generations in seven different environments. We measured the competitive fitness of all ancestral and evolved lines against a common competitor and find that in all seven environments, haploid lines adapted faster than diploids, significantly so in three environments. We apply theory that relates the rates of adaptation and measured effective population sizes to the properties of beneficial mutations. We obtained rough estimates of the average selection coefficients in haploids between 2% and 10% for these first selected mutations. Results were consistent with semi-dominant to dominant mutations in four environments and recessive to additive mutations in two other environments. These results are consistent with theory that predicts haploids should evolve faster than diploids at large population sizes.     

Rapid adaptation to a novel host in a seed beetle (Callosobruchus maculatus): the role of sexual selection

Rapid diversification is common among herbivorous insects and is often the result of host shifts, leading to the exploitation of novel food sources. This, in turn, is associated with adaptive evolution of female oviposition behavior and larval feeding biology. Although natural selection is the typical driver of such adaptation, the role of sexual selection is less clear. In theory, sexual selection can either accelerate or impede adaptation. To assess the independent effects of natural and sexual selection on the rate of adaptation, we performed a laboratory natural selection experiment in a herbivorous bruchid beetle (Callosobruchus maculatus). We established replicated selection lines where we varied natural (food type) and sexual (mating system) selection in a 2 x 2 orthogonal design, and propagated our lines for 35 generations. In half of the lines, we induced a host shift whereas the other half was kept on the ancestral host. We experimentally enforced monogamy in half of the lines, whereas the other half remained polygamous. The beetles rapidly adapted to the novel host, which primarily involved increased host acceptance by females and an accelerated rate of larval development. We also found that our mating system treatment affected the rate of adaptation, but that this effect was contingent upon food type. As beetles adapted to the novel host, sexual selection reinforced natural selection whereas populations residing close to their adaptive peak (i.e., those using their ancestral host) exhibited higher fitness in the absence of sexual selection. We discuss our findings in light of current sexual selection theory and suggest that the net evolutionary effect of reproductive competition may critically depend on natural selection. Sexual selection may commonly accelerate adaptation under directional natural selection whereas sexual selection, and the associated load brought by sexual conflict, may tend to depress population fitness under stabilizing natural selection.     

Adaptive divergence in body size overrides the effects of plasticity across natural habitats in the brown trout

The evolution of life-history traits is characterized by trade-offs between different selection pressures, as well as plasticity across environmental conditions. Yet, studies on local adaptation are often performed under artificial conditions, leaving two issues unexplored: (i) how consistent are laboratory inferred local adaptations under natural conditions and (ii) how much phenotypic variation is attributed to phenotypic plasticity and to adaptive evolution, respectively, across environmental conditions? We reared fish from six locally adapted (domesticated and wild) populations of anadromous brown trout (Salmo trutta) in one semi-natural and three natural streams and recorded a key life-history trait (body size at the end of first growth season). We found that population-specific reaction norms were close to parallel across different streams and Q_ST was similar – and larger than F_ST – within all streams, indicating a consistency of local adaptation in body size across natural environments. The amount of variation explained by population origin exceeded the variation across stream environments, indicating that genetic effects derived from adaptive processes have a stronger effect on phenotypic variation than plasticity induced by environmental conditions. These results suggest that plasticity does not “swamp” the phenotypic variation, and that selection may thus be efficient in generating genetic change.     

Reverse evolution of fitness in Drosophila melanogaster

Abstract The evolution of fitness is central to evolutionary theory, yet few experimental systems allow us to track its evolution in genetically and environmentally relevant contexts. Reverse evolution experiments allow the study of the evolutionary return to ancestral phenotypic states, including fitness. This in turn permits well‐defined tests for the dependence of adaptation on evolutionary history and environmental conditions. In the experiments described here, 20 populations of heterogeneous evolutionary histories were returned to their common ancestral environment for 50 generations, and were then compared with both their immediate differentiated ancestors and populations which had remained in the ancestral environment. One measure of fitness returned to ancestral levels to a greater extent than other characters did. The phenotypic effects of reverse evolution were also contingent on previous selective history. Moreover, convergence to the ancestral state was highly sensitive to environmental conditions. The phenotypic plasticity of fecundity, a character directly selected for, evolved during the experimental time frame. Reverse evolution appears to force multiple, diverged populations to converge on a common fitness state through different life‐history and genetic changes.     

Loss of adaptation following reversion suggests trade‐offs in host use by a seed beetle

Experimental evolution has provided little support for the hypothesis that the narrow diets of herbivorous insects reflect trade‐offs in performance across hosts; selection lines can sometimes adapt to an inferior novel host without a decline in performance on the ancestral host. An alternative approach for detecting trade‐offs would be to measure adaptation decay after selection is relaxed, that is, when populations newly adapted to a novel host are reverted to the ancestral one. Lines of the seed beetle Callosobruchus maculatus rapidly adapted to a poor host (lentil); survival in lentil seeds increased from 2% to > 90% in < 30 generations. After the lines had reached a plateau with respect to survival in lentil, sublines were reverted to the ancestral host, mung bean. Twelve generations of reversion had little effect on performance in lentil, but after 25–35 generations, the reverted lines exhibited lower survival, slower development and smaller size. The most divergent pair of lines was then assayed on both lentil and mung bean. Performance on lentil was again much poorer in the reverted line than in the nonreverted one, but the lines performed equally well on mung bean. Moreover, the performance of the nonreverted line on mung bean remained comparable to that of the original mung‐bean population. Our results thus present a paradox: loss of adaptation to lentil following reversion implies a trade‐off, but the continued strong performance of lentil‐adapted lines on mung bean does not. Genomic comparisons of the reverted, nonreverted and ancestral lines may resolve this paradox and determine the importance of selection vs. drift in causing a loss of adaptation following reversion.     

Predictable modification of body size and competitive ability following a host shift by a seed beetle

Interfertile populations of the seed beetle Callosobruchus maculatus differ genetically in several behavioral, morphological, and life-history traits, including traits that affect the intensity of larval competition within seeds. Previous studies have suggested that this variation depends on differences in host size. I performed a selection experiment in which replicate beetle lines were either maintained on a small, ancestral host (mung bean) or switched to a larger, novel host (cowpea). After 40 generations, I estimated survival, development time, and adult mass on each host, both in the presence and absence of larval competition. The shift to cowpea substantially reduced body size; irrespective of rearing host, adults from the cowpea lines were more than 10% lighter than those from the mung bean lines. Switching to cowpea also improved survival and reduced development time on this host, but without decreasing performance on the ancestral host. The most striking effect of the shift to a larger host was a reduction in larval competitiveness. When two even-aged larvae co-existed within a seed, the probability that both survived to adult emergence was > or = 65% if larvae were from the cowpea lines but < or = 12% if they were from the mung bean lines. The adverse effects of competition on development time and adult mass were also less severe in the cowpea lines than in the mung bean lines. By rapidly evolving smaller size and reduced competitiveness, the cowpea lines converged toward populations chronically associated with cowpea. These results suggest that evolutionary trajectories can be predictable, and that host-specific selection can play a major role in the diversification of insect life histories. Because host shifts by small, endophagous insects are comparable to the colonization of new habitats, adaptive responses may often include traits (such as larval competitiveness) that are not directly related to host use.     

Life history trade-offs and relaxed selection can decrease bacterial virulence in environmental reservoirs

Pathogen virulence is usually thought to evolve in reciprocal selection with the host. While this might be true for obligate pathogens, the life histories of opportunistic pathogens typically alternate between within-host and outside-host environments during the infection-transmission cycle. As a result, opportunistic pathogens are likely to experience conflicting selection pressures across different environments, and this could affect their virulence through life-history trait correlations. We studied these correlations experimentally by exposing an opportunistic bacterial pathogen Serratia marcescens to its natural protist predator Tetrahymena thermophila for 13 weeks, after which we measured changes in bacterial traits related to both anti-predator defence and virulence. We found that anti-predator adaptation (producing predator-resistant biofilm) caused a correlative attenuation in virulence. Even though the direct mechanism was not found, reduction in virulence was most clearly connected to a predator-driven loss of a red bacterial pigment, prodigiosin. Moreover, life-history trait evolution was more divergent among replicate populations in the absence of predation, leading also to lowered virulence in some of the 'predator absent' selection lines. Together these findings suggest that the virulence of non-obligatory, opportunistic bacterial pathogens can decrease in environmental reservoirs through life history trade-offs, or random accumulation of mutations that impair virulence traits under relaxed selection.     

The genetic covariance among clinal environments after adaptation to an environmental gradient in Drosophila serrata

We examined the genetic basis of clinal adaptation by determining the evolutionary response of life-history traits to laboratory natural selection along a gradient of thermal stress in Drosophila serrata. A gradient of heat stress was created by exposing larvae to a heat stress of 36 degrees for 4 hr for 0, 1, 2, 3, 4, or 5 days of larval development, with the remainder of development taking place at 25 degrees. Replicated lines were exposed to each level of this stress every second generation for 30 generations. At the end of selection, we conducted a complete reciprocal transfer experiment where all populations were raised in all environments, to estimate the realized additive genetic covariance matrix among clinal environments in three life-history traits. Visualization of the genetic covariance functions of the life-history traits revealed that the genetic correlation between environments generally declined as environments became more different and even became negative between the most different environments in some cases. One exception to this general pattern was a life-history trait representing the classic trade-off between development time and body size, which responded to selection in a similar genetic fashion across all environments. Adaptation to clinal environments may involve a number of distinct genetic effects along the length of the cline, the complexity of which may not be fully revealed by focusing primarily on populations at the ends of the cline.     

Effects of the [PSI+] prion on rates of adaptation in yeast

The [PSI(+)] prion in yeast has been shown to improve short-term growth in some environments, but its effects on rates of adaptation have not been assessed before now. We adapted three yeast genotypes to three novel environments in the presence and the absence of the prion. There were significant differences in adaptation rates between lines with different combinations of genotype, environment, and prion status. We saw no consistent effect, however, of the prion on the rate of adaptation to new environments. A major factor affecting the rate of adaptation was initial fitness in the new environment: lines with low initial fitness evolved faster than lines with high initial fitness.     

Experimental evolution of resistance in Paramecium caudatum against the bacterial parasite Holospora undulata

Host-parasite coevolution is often described as a process of reciprocal adaptation and counter adaptation, driven by frequency-dependent selection. This requires that different parasite genotypes perform differently on different host genotypes. Such genotype-by-genotype interactions arise if adaptation to one host (or parasite) genotype reduces performance on others. These direct costs of adaptation can maintain genetic polymorphism and generate geographic patterns of local host or parasite adaptation. Fixation of all-resistant (or all-infective) genotypes is further prevented if adaptation trades off with other host (or parasite) life-history traits. For the host, such indirect costs of resistance refer to reduced fitness of resistant genotypes in the absence of parasites. We studied (co)evolution in experimental microcosms of several clones of the freshwater protozoan Paramecium caudatum, infected with the bacterial parasite Holospora undulata. After two and a half years of culture, inoculation of evolved and naive (never exposed to the parasite) hosts with evolved and founder parasites revealed an increase in host resistance, but not in parasite infectivity. A cross-infection experiment showed significant host clone-by-parasite isolate interactions, and evolved hosts tended to be more resistant to their own (local) parasites than to parasites from other hosts. Compared to naive clones, evolved host clones had lower division rates in the absence of the parasite. Thus, our study indicates de novo evolution of host resistance, associated with both direct and indirect costs. This illustrates how interactions with parasites can lead to the genetic divergence of initially identical populations.     

Influence of genetic architecture on contemporary local evolution in the soapberry bug,Jadera haematoloma: artificial selection on beak length

Little is known about the influence of genetic architecture on local adaptation. We investigated the genetic architecture of the rapid contemporary evolution of mouthparts, the flight polymorphism and life history traits in the soapberry bug Jadera haematoloma (Hemiptera) using laboratory selection. The mouthparts of these seed‐feeding bugs have adapted in 40–50 years by decreasing in length following novel natural selection induced by a host switch to the seeds of an introduced tree with smaller fruits than those of the native host vine. Laboratory selection on beak length in both an ancestral population feeding on the native host and a derived population feeding on the introduced host reveals genetic variance allowing a rapid response (heritabilities of 0.51–0.87) to selection for either longer or shorter beaks. This selection resulted in reverse evolution by restoring long beaks in the derived population and forward evolution by re‐creating short beaks in the ancestral bugs. There were strong genetic correlations (0.68–0.84) in both populations between beak lengths and the frequency of flight morphs, with short beaks associated with short wings. The results reveal a genetically interrelated set of adaptive multivariate traits including both beak length and flight morph. This suite of traits reflects host plant patchiness and seeding phenology. Weaker evidence suggests that egg mass and early egg production may be elements of the same suite. Reversible or forward evolution thus may occur in a broad set of genetically correlated multivariate traits undergoing rapid contemporary adaptation to altered local environments.     

Ancestral population reconstitution from isofemale lines as a tool for experimental evolution

Experimental evolution is a powerful tool to study adaptation under controlled conditions. Laboratory natural selection experiments mimic adaptation in the wild with better‐adapted genotypes having more offspring. Because the selected traits are frequently not known, adaptation is typically measured as fitness increase by comparing evolved populations against an unselected reference population maintained in a laboratory environment. With adaptation to the laboratory conditions and genetic drift, however, it is not clear to what extent such comparisons provide unbiased estimates of adaptation. Alternatively, ancestral variation could be preserved in isofemale lines that can be combined to reconstitute the ancestral population. Here, we assess the impact of selection on alleles segregating in newly established Drosophila isofemale lines. We reconstituted two populations from isofemale lines and compared them to two original ancestral populations (AP) founded from the same lines shortly after collection. No significant allele frequency changes could be detected between both AP and simulations showed that drift had a low impact compared to Pool‐Seq‐associated sampling effects. We conclude that laboratory selection on segregating variation in isofemale lines is too weak to have detectable effects, which validates ancestral population reconstitution from isofemale lines as an unbiased approach for measuring adaptation in evolved populations.