Coevolution of competing Callosobruchus species does not stabilize coexistence

Interspecific resource competition is expected to select for divergence in resource use, weakening interspecific relative to intraspecific competition, thus promoting stable coexistence. More broadly, because interspecific competition reduces fitness, any mechanism of interspecific competition should generate selection favoring traits that weaken interspecific competition. However, species also can adapt to competition by increasing their competitive ability, potentially destabilizing coexistence. We reared two species of bean beetles, the specialist Callosobruchus maculatus and the generalist C. chinensis, in allopatry and sympatry on a mixture of adzuki beans and lentils, and assayed mutual invasibility after four, eight, and twelve generations of evolution. Contrary to the expectation that coevolution of competitors will weaken interspecific competition, the rate of mutual invasibility did not differ between sympatry and allopatry. Rather, the invasion rate of C. chinensis, but not C. maculatus, increased with duration of evolution, as C. chinensis adapted to lentils without experiencing reduced adaptation to adzuki beans, and regardless of the presence or absence of C. maculatus. Our results highlight that evolutionary responses to interspecific competition promote stable coexistence only under specific conditions that can be difficult to produce in practice.     

Low concordance of short‐term and long‐term selection responses in experimental Drosophila populations

Experimental evolution is becoming a popular approach to study the genomic selection response of evolving populations. Computer simulation studies suggest that the accuracy of the signature increases with the duration of the experiment. Since some assumptions of the computer simulations may be violated, it is important to scrutinize the influence of the experimental duration with real data. Here, we use a highly replicated Evolve and Resequence study in Drosophila simulans to compare the selection targets inferred at different time points. At each time point, approximately the same number of SNPs deviates from neutral expectations, but only 10% of the selected haplotype blocks identified from the full data set can be detected after 20 generations. Those haplotype blocks that emerge already after 20 generations differ from the others by being strongly selected at the beginning of the experiment and display a more parallel selection response. Consistent with previous computer simulations, our results demonstrate that only Evolve and Resequence experiments with a sufficient number of generations can characterize complex adaptive architectures.     

Nonlinear frequency‐dependent selection promotes long‐term coexistence between bacteria species

Negative frequency‐dependent selection (NFDS) is an important mechanism for species coexistence and for the maintenance of genetic polymorphism. Long‐term coexistence nevertheless requires NFDS interactions to be resilient to further evolution of the interacting species or genotypes. For closely related genotypes, NFDS interactions have been shown to be preserved through successive rounds of evolution in coexisting lineages. On the contrary, the evolution of NFDS interactions between distantly related species has received less attention. Here, we tracked the co‐evolution of Escherichia coli and Citrobacter freundii that initially differ in their ecological characteristics. We showed that these two bacterial species engaged in an NFDS interaction particularly resilient to further evolution: despite a very strong asymmetric rate of adaptation, their coexistence was maintained owing to an NFDS pattern where fitness increases steeply as the frequency decreases towards zero. Using a model, we showed how and why such NFDS pattern can emerge. These findings provide a robust explanation for the long‐term maintenance of species at very low frequencies.     

Evolution of larval competitiveness and associated life‐history traits in response to host shifts in a seed beetle

Resource competition is frequently strong among parasites that feed within small discrete resource patches, such as seeds or fruits. The properties of a host can influence the behavioural, morphological and life‐history traits of associated parasites, including traits that mediate competition within the host. For seed parasites, host size may be an especially important determinant of competitive ability. Using the seed beetle, Callosobruchus maculatus, we performed replicated, reciprocal host shifts to examine the role of seed size in determining larval competitiveness and associated traits. Populations ancestrally associated with either a small host (mung bean) or a large one (cowpea) were switched to each other's host for 36 generations. Compared to control lines (those remaining on the ancestral host), lines switched from the small host to the large host evolved greater tolerance of co‐occurring larvae within seeds (indicated by an increase in the frequency of small seeds yielding two adults), smaller egg size and higher fecundity. Each change occurred in the direction predicted by the traits of populations already adapted to cowpea. However, we did not observe the expected decline in adult mass following the shift to the larger host. Moreover, lines switched from the large host (cowpea) to the small host (mung bean) did not evolve the predicted increase in larval competitiveness or egg size, but did exhibit the predicted increase in body mass. Our results thus provide mixed support for the hypothesis that host size determines the evolution of competition‐related traits of seed beetles. Evolutionary responses to the two host shifts were consistent among replicate lines, but the evolution of larval competition was asymmetric, with larval competitiveness evolving as predicted in one direction of host shift, but not the reverse. Nevertheless, our results indicate that switching hosts is sufficient to produce repeatable and rapid changes in the competition strategy and fitness‐related traits of insect populations.     

Multi‐stage disruption of freshwater mussel reproduction by high suspended solids in short‐ and long‐term brooders

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Experimental evolution reveals habitat‐specific fitness dynamics among Wolbachia clades in Drosophila melanogaster

The diversity and infection dynamics of the endosymbiont Wolbachia can be influenced by many factors, such as transmission rate, cytoplasmic incompatibility, environment, selection and genetic drift. The interplay of these factors in natural populations can result in heterogeneous infection patterns with substantial differences between populations and strains. The causes of these heterogeneities are not yet understood, partly due to the complexity of natural environments. We present experimental evolution as a new approach to study Wolbachia infection dynamics in replicate populations exposed to a controlled environment. A natural Drosophila melanogaster population infected with strains of Wolbachia belonging to different clades evolved in two laboratory environments (hot and cold) for 1.5 years. In both treatments, the rate of Wolbachia infection increased until fixation. In the hot environment, the relative frequency of different Wolbachia clades remained stable over 37 generations. In the cold environment, however, we observed marked changes in the composition of the Wolbachia population: within 15 generations, one Wolbachia clade increased more than 50% in frequency, whereas the other two clades decreased in frequency, resulting in the loss of one clade. The frequency change was highly reproducible not only among replicates, but also when flies that evolved for 42 generations in the hot environment were transferred to the cold environment. These results document how environmental factors can affect the composition of Wolbachia in D. melanogaster. The high reproducibility of the pattern suggests that experimental evolution studies can efficiently determine the functional basis of habitat‐specific fitness among Wolbachia strains.     

Genetic assignment of recruits reveals short‐ and long‐distance larval dispersal in Pocillopora damicornis on the Great Barrier Reef

Understanding connectivity of coral populations among and within reefs over ecologically significant timescales is essential for developing evidence‐based management strategies, including the design of marineprotected areas. Here, we present the first assessment of contemporary connectivity among populations of two Molecular Operational Taxonomic Units (MOTUs) of the brooding coral Pocillopora damicornis. We used individual‐based genetic assignment methods to identify the proportions of philopatric and migrant larval recruits, settling over 12 months at sites around Lizard Island (northern Great Barrier Reef [GBR]) and over 24 months at sites around the Palms Islands (central GBR). Overall, we found spatially and temporally variable rates of self‐recruitment and dispersal, demonstrating the importance of variation in local physical characteristics in driving dispersal processes. Recruitment patterns and inferred dispersal distances differed between the two P. damicornis MOTUs, with type α recruits exhibiting predominantly philopatric recruitment, while the majority of type β recruits were either migrants from identified putative source populations or assumed migrants based on genetic exclusion from all known populations. While P. damicornis invests much energy into brooding clonal larvae, we found that only 15% and 7% of type α and type β recruits, respectively, were clones of sampled adult colonies or other recruits, challenging the hypothesis that reproduction is predominantly asexual in this species on the GBR. We explain high rates of self‐recruitment and low rates of clonality in these MOTUs by suggesting that locally retained larvae originate predominantly from spawned gametes, while brooded larvae are mainly vagabonds.     

Sperm competition generates evolution of increased paternal investment in a sex role‐reversed seed beetle

When males provide females with resources at mating, they can become the limiting sex in reproduction, in extreme cases leading to the reversal of typical courtship roles. The evolution of male provisioning is thought to be driven by male reproductive competition and selection for female fecundity enhancement. We used experimental evolution under male‐ or female‐biased sex ratios and limited or unlimited food regimes to investigate the relative roles of these routes to male provisioning in a sex role‐reversed beetle, Megabruchidius tonkineus, where males provide females with nutritious ejaculates. Males evolving under male‐biased sex ratios transferred larger ejaculates than did males from female‐biased populations, demonstrating a sizeable role for reproductive competition in the evolution of male provisioning. Although larger ejaculates elevated female lifetime offspring production, we found little evidence of selection for larger ejaculates via fecundity enhancement: males evolving under resource‐limited and unlimited conditions did not differ in mean ejaculate size. Resource limitation did, however, affect the evolution of conditional ejaculate allocation. Our results suggest that the resource provisioning that underpins sex role reversal in this system is the result of male–male reproductive competition rather than of direct selection for males to enhance female fecundity.     

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.     

Phylogeny and species delineation in the marine diatom Pseudo‐nitzschia (Bacillariophyta) using cox1, LSU,and ITS2 rRNA genes: A perspective in character evolution

Analyses of the mitochondrial cox1, the nuclear‐encoded large subunit (LSU), and the internal transcribed spacer 2 (ITS2) RNA coding region of Pseudo‐nitzschia revealed that the P. pseudodelicatissima complex can be phylogenetically grouped into three distinct clades (Groups I–III), while the P. delicatissima complex forms another distinct clade (Group IV) in both the LSU and ITS2 phylogenetic trees. It was elucidated that comprehensive taxon sampling (sampling of sequences), selection of appropriate target genes and outgroup, and alignment strategies influenced the phylogenetic accuracy. Based on the genetic divergence, ITS2 resulted in the most resolved trees, followed by cox1 and LSU. The morphological characters available for Pseudo‐nitzschia, although limited in number, were overall in agreement with the phylogenies when mapped onto the ITS2 tree. Information on the presence/absence of a central nodule, number of rows of poroids in each stria, and of sectors dividing the poroids mapped onto the ITS2 tree revealed the evolution of the recently diverged species. The morphologically based species complexes showed evolutionary relevance in agreement with molecular phylogeny inferred from ITS2 sequence–structure data. The data set of the hypervariable region of ITS2 improved the phylogenetic inference compared to the cox1 and LSU data sets. The taxonomic status of P. cuspidata and P. pseudodelicatissima requires further elucidation.     

Using genomic data to revisit an early example of reproductive character displacement in Haitian Anolis lizards

The pattern of reproductive character displacement (RCD)—in which traits associated with reproductive isolation are more different where two species occur together than where they occur in isolation—is frequently attributed to reinforcement, a process during which natural selection acting against maladaptive mating events leads to enhanced prezygotic isolation between species or incipient species. One of the first studies of RCD to include molecular genetic data was described 40 years ago in a complex of Haitian trunk anole lizards using a small number of allozyme loci. In this example, Anolis caudalis appears to experience divergence in the color and pattern of an extensible throat fan, or dewlap, in areas of contact with closely related species at the northern and southern limits of its range. However, this case study has been largely overlooked for decades; meanwhile, explanations for geographic variation in dewlap color and pattern have focused primarily on adaptation to local signalling environments. We reinvestigate this example using amplified fragment length polymorphism (AFLP) genome scans, mtDNA sequence data, information on dewlap phenotypes and GIS data on environmental variation to test the hypothesis of RCD generated by reinforcement in Haitian trunk anoles. Together, our phenotypic and genetic results are consistent with RCD at the southern and northern limits of the range of A. caudalis. We evaluate the evidence for reinforcement as the explanation for RCD in Haitian trunk anoles, consider alternative explanations and provide suggestions for future work on the relationship between dewlap variation and speciation in Haitian trunk anoles.     

Long‐term continental changes in wing length,but not bill length,of a long‐distance migratory shorebird

We compiled a >50‐year record of morphometrics for semipalmated sandpipers (Calidris pusilla), a shorebird species with a Nearctic breeding distribution and intercontinental migration to South America. Our data included >57,000 individuals captured 1972–2015 at five breeding locations and three major stopover sites, plus 139 museum specimens collected in earlier decades. Wing length increased by ca. 1.5 mm (>1%) prior to 1980, followed by a decrease of 3.85 mm (nearly 4%) over the subsequent 35 years. This can account for previously reported changes in metrics at a migratory stopover site from 1985 to 2006. Wing length decreased at a rate of 1,098 darwins, or 0.176 haldanes, within the ranges of other field studies of phenotypic change. Bill length, in contrast, showed no consistent change over the full period of our study. Decreased body size as a universal response of animal populations to climate warming, and several other potential mechanisms, are unable to account for the increasing and decreasing wing length pattern observed. We propose that the post‐WWII near‐extirpation of falcon populations and their post‐1973 recovery driven by the widespread use and subsequent limitation on DDT in North America selected initially for greater flight efficiency and latterly for greater agility. This predation danger hypothesis accounts for many features of the morphometric data and deserves further investigation in this and other species.     

Temperature sensitivity of biomass‐specific microbial exo‐enzyme activities and CO2 efflux is resistant to change across short‐ and long‐term timescales

Accurate representation of temperature sensitivity (Q₁₀) of soil microbial activity across time is critical for projecting soil CO₂ efflux. As microorganisms mediate soil carbon (C) loss via exo‐enzyme activity and respiration, we explore temperature sensitivities of microbial exo‐enzyme activity and respiratory CO₂ loss across time and assess mechanisms associated with these potential changes in microbial temperature responses. We collected soils along a latitudinal boreal forest transect with different temperature regimes (long‐term timescale) and exposed these soils to laboratory temperature manipulations at 5, 15, and 25°C for 84 days (short‐term timescale). We quantified temperature sensitivity of microbial activity per g soil and per g microbial biomass at days 9, 34, 55, and 84, and determined bacterial and fungal community structure before the incubation and at days 9 and 84. All biomass‐specific rates exhibited temperature sensitivities resistant to change across short‐ and long‐term timescales (mean Q₁₀ = 2.77 ± 0.25, 2.63 ± 0.26, 1.78 ± 0.26, 2.27 ± 0.25, 3.28 ± 0.44, 2.89 ± 0.55 for β‐glucosidase, N‐acetyl‐β‐d ‐glucosaminidase, leucine amino peptidase, acid phosphatase, cellobiohydrolase, and CO₂ efflux, respectively). In contrast, temperature sensitivity of soil mass‐specific rates exhibited either resilience (the Q₁₀ value changed and returned to the original value over time) or resistance to change. Regardless of the microbial flux responses, bacterial and fungal community structure was susceptible to change with temperature, significantly differing with short‐ and long‐term exposure to different temperature regimes. Our results highlight that temperature responses of microbial resource allocation to exo‐enzyme production and associated respiratory CO₂ loss per unit biomass can remain invariant across time, and thus, that vulnerability of soil organic C stocks to rising temperatures may persist in the long term. Furthermore, resistant temperature sensitivities of biomass‐specific rates in spite of different community structures imply decoupling of community constituents and the temperature responses of soil microbial activities.     

Influence of short‐term drought conditions and subsequent re‐watering on the physiology and proteome of Lolium multiflorum/Festuca arundinacea introgression forms,with contrasting levels of tolerance to long‐term drought

Festuca arundinacea is a drought tolerant species. Lolium multiflorum has better forage quality but lower tolerance to abiotic stresses. Their hybrids offer an opportunity to perform research on the molecular basis of tolerance to drought. The aim of this work was to recognise the mechanisms of response to short‐term drought (11 days) in a glasshouse in two L. multiflorum/F. arundinacea introgression forms with distinct levels of tolerance to long‐term drought (14 weeks) in the field. Measurements of physiological parameters, analyses of protein accumulation profiles using two‐dimensional gel electrophoresis, and mass spectrometry identification of proteins, which were accumulated differentially between the selected genotypes during short‐term drought, were performed. Genotype 7/6, with lower yield potential during 14 weeks of drought, and lower ability to re‐grow after watering, had a higher capacity for photosynthesis during 11 days of drought. Genotype 4/10, more tolerant to long‐term drought, was able to repair damaged cell membranes after watering and was also characterised by lower transpiration during short‐term drought. A total of 455 proteins were analysed, and the 17 that were differentially accumulated between the two genotypes were identified. The results of physiological and proteomic research led to a hypothesis that the higher photosynthetic capacity of genotype 7/6 could be due to a more efficient Calvin cycle, supported by higher accumulation of crucial proteins involving chloroplast aldolase.     

The effectiveness of short‐term fox control in protecting a seasonally vulnerable species,the Eastern Long‐necked Turtle (Chelodina longicollis)

Reducing predation by introduced predators on seasonally vulnerable prey is of interest to biodiversity and game managers around the world. In Australia, the Red Fox (Vulpes vulpes) is a significant predator of freshwater turtle nests, destroying up to 93% of nests. We used a nonrandomized intervention study to assess the effectiveness of a short‐term (3‐week) but broad‐scale baiting operation in reducing the level of nest predation on artificial turtle nests around a complex lake system during a major flooding event in north‐western Victoria. Estimates of fox occupancy declined from 0.58 (0.44–0.70 95% CI) to 0.34 (0.21–0.46 95% CI) following fox control. Modelling of nest‐survival rates indicated there was no significant change in survival rates. Effective short‐term predator control to protect seasonally vulnerable prey is desirable and achievable. Knowledge of underlying predator density, predator–bait encounter and consumption rates, and the optimal duration of short‐term control is needed to reduce the risk to prey.     

Phylogenomic analysis of gene co‐expression networks reveals the evolution of functional modules

Molecular evolutionary studies correlate genomic and phylogenetic information with the emergence of new traits of organisms. These traits are, however, the consequence of dynamic gene networks composed of functional modules, which might not be captured by genomic analyses. Here, we established a method that combines large‐scale genomic and phylogenetic data with gene co‐expression networks to extensively study the evolutionary make‐up of modules in the moss Physcomitrella patens, and in the angiosperms Arabidopsis thaliana and Oryza sativa (rice). We first show that younger genes are less annotated than older genes. By mapping genomic data onto the co‐expression networks, we found that genes from the same evolutionary period tend to be connected, whereas old and young genes tend to be disconnected. Consequently, the analysis revealed modules that emerged at a specific time in plant evolution. To uncover the evolutionary relationships of the modules that are conserved across the plant kingdom, we added phylogenetic information that revealed duplication and speciation events on the module level. This combined analysis revealed an independent duplication of cell wall modules in bryophytes and angiosperms, suggesting a parallel evolution of cell wall pathways in land plants. We provide an online tool allowing plant researchers to perform these analyses at http://www.gene2function.de .     

Long‐term evolution of the natural isolate of Escherichia coli 536 in the mouse gut colonized after maternal transmission reveals convergence in the constitutive expression of the lactose operon

In vitro experimental evolution has taught us many lessons on the molecular bases of adaptation. To move towards more natural settings, evolution in the mice gut has been successfully performed. Yet, these experiments suffered from the use of laboratory strains as well as the use of axenic or streptomycin‐treated mice to maintain the inoculated strains. To circumvent these limitations, we conducted a one‐year experimental evolution in vivo using a natural isolate of E. coli, strain 536, in conditions mimicking as much as possible natural environment with mother‐to‐offspring microbiota transmission. Mice were then distributed in 24 independent cages and separated into two different diets: a regular one (chow diet, CD) and high‐fat and high‐sugar one (Western Diet, WD). Genome sequences revealed an early and rapid selection during the breastfeeding period that selected the constitutive expression of the well‐characterized lactose operon. E. coli was lost significantly more in CD than WD; however, we could not detect any genomic signature of selection, nor any diet specificities during the later part of the experiments. The apparently neutral evolution presumably due to low population size maintained nevertheless at high frequency the early selected mutations affecting lactose regulation. The rapid loss of lactose operon regulation challenges the idea that plastic gene expression is both optimal and stable in the wild.     

Climatic and biotic extreme events moderate long‐term responses of above‐ and belowground sub‐Arctic heathland communities to climate change

Climate change impacts are not uniform across the Arctic region because interacting factors causes large variations in local ecosystem change. Extreme climatic events and population cycles of herbivores occur simultaneously against a background of gradual climate warming trends and can redirect ecosystem change along routes that are difficult to predict. Here, we present the results from sub‐Arctic heath vegetation and its belowground micro‐arthropod community in response to the two main drivers of vegetation damage in this region: extreme winter warming events and subsequent outbreaks of the defoliating autumnal moth caterpillar (Epirrita autumnata). Evergreen dwarf shrub biomass decreased (30%) following extreme winter warming events and again by moth caterpillar grazing. Deciduous shrubs that were previously exposed to an extreme winter warming event were not affected by the moth caterpillar grazing, while those that were not exposed to warming events (control plots) showed reduced (23%) biomass from grazing. Cryptogam cover increased irrespective of grazing or winter warming events. Micro‐arthropods declined (46%) following winter warming but did not respond to changes in plant community. Extreme winter warming and caterpillar grazing suppressed the CO₂ fluxes of the ecosystem. Evergreen dwarf shrubs are disadvantaged in a future sub‐Arctic with more stochastic climatic and biotic events. Given that summer warming may further benefit deciduous over evergreen shrubs, event and trend climate change may both act against evergreen shrubs and the ecosystem functions they provide. This is of particular concern given that Arctic heath vegetation is typically dominated by evergreen shrubs. Other components of the vegetation showed variable responses to abiotic and biotic events, and their interaction indicates that sub‐Arctic vegetation response to multiple pressures is not easy to predict from single‐factor responses. Therefore, while biotic and climatic events may have clear impacts, more work is needed to understand their net effect on Arctic ecosystems.