Maternal epigenetic pathways control parental contributions to Arabidopsis early embryogenesis.

Defining the contributions and interactions of paternal and maternal genomes during embryo development is critical to understand the fundamental processes involved in hybrid vigor, hybrid sterility, and reproductive isolation. To determine the parental contributions and their regulation during Arabidopsis embryogenesis, we combined deep-sequencing-based RNA profiling and genetic analyses. At the 2-4 cell stage there is a strong, genome-wide dominance of maternal transcripts, although transcripts are contributed by both parental genomes. At the globular stage the relative paternal contribution is higher, largely due to a gradual activation of the paternal genome. We identified two antagonistic maternal pathways that control these parental contributions. Paternal alleles are initially downregulated by the chromatin siRNA pathway, linked to DNA and histone methylation, whereas transcriptional activation requires maternal activity of the histone chaperone complex CAF1. Our results define maternal epigenetic pathways controlling the parental contributions in plant embryos, which are distinct from those regulating genomic imprinting.

The Origin of Asexual Brine Shrimps.

AbstractDetermining how and how often asexual lineages emerge within sexual species is central to our understanding of sex-asex transitions and the long-term maintenance of sex. Asexuality can arise "by transmission" from an existing asexual lineage to a new one through different types of crosses. The occurrence of these crosses, cryptic sex, variations in ploidy, and recombination within asexuals greatly complicates the study of sex-asex transitions, as they preclude the use of standard phylogenetic methods and genetic distance metrics. In this study we show how to overcome these challenges by developing new approaches to investigate the origin of the various asexual lineages of the brine shrimp Artemia parthenogenetica. We use a large sample of asexuals, including all known polyploids, and their sexual relatives. We combine flow cytometry with mitochondrial and nuclear DNA data. We develop new genetic distance measures and methods to compare various scenarios describing the origin of the different lineages. We find that all diploid and polyploid A. parthenogenetica likely arose within the past 80,000 years through successive and nested hybridization events that involved backcrosses with different sexual species. All A. parthenogenetica have the same common ancestor and therefore likely carry the same asexuality gene(s) and reproduce by automixis. These findings radically change our view of sex-asex transitions in this group and show the importance of considering scenarios of asexuality by transmission. The methods developed are applicable to many other asexual taxa.

Trait-specific trade-offs prevent niche expansion in two parasites.

It is often difficult to determine why parasites do not evolve broader niches, especially when there are closely related and ecologically similar hosts available. We used an experimental evolution approach to test whether source-sink demography or trade-offs drive specialization, and its underlying traits, in two microsporidian parasites infecting two brine shrimp species. In the field, both parasites regularly infect both hosts, but experiments have shown that they are partially specialized. We serially passaged the parasites on one, the other, or an alternation of the two hosts; after 10 passages, we assayed the infectivity, virulence, and spore production of the evolved lines. Our results indicated a weak between-host trade-off acting on infectivity, but a strong trade-off acting on spore production. Consequently, spore production maintained both parasites' overall pattern of specialization. This study highlights that when trade-off shapes differ among traits, one key trait can prevent the evolution of generalism.

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.

Dividing a Maternal Pie among Half-Sibs: Genetic Conflicts and the Control of Resource Allocation to Seeds in Maize.

Resource allocation to offspring is the battleground for various intrafamilial conflicts. Understanding these conflicts requires knowledge of how the different actors (mother, siblings with different paternal genotypes) influence resource allocation. In angiosperms, allocation of resources to seeds happens postfertilization, and the paternally inherited genome in offspring can therefore influence resource allocation. However, the precise mode of resource allocation-and, in particular, the occurrence of sibling rivalry-has rarely been investigated in plants. In this article, we develop a new method for analyzing the resource-allocation traits of the different actors (maternal sporophyte and half-sibs) using data obtained from a large-scale diallel cross experiment in maize involving mixed hand pollination and color markers to assess seed weight of known paternity. We found strong evidence for the occurrence of sibling rivalry: resources invested in an ear were allocated competitively, and offspring with different paternal genotypes aggressively competed for these resources, entailing a measurable direct cost to the mother. We also show how resource allocation can be described for each genotype by two maternal traits (source effect, average sink responsiveness) and two offspring traits (ability to attract maternal resources, competitive ability toward siblings). We will discuss how these findings help to understand how genetic conflicts shape resource-allocation traits in angiosperms.

When Parasites Are Good for Health: Cestode Parasitism Increases Resistance to Arsenic in Brine Shrimps.

Parasites and pollutants can both affect any living organism, and their interactions can be very important. To date, repeated studies have found that parasites and heavy metals or metalloids both have important negative effects on the health of animals, often in a synergistic manner. Here, we show for the first time that parasites can increase host resistance to metalloid arsenic, focusing on a clonal population of brine shrimp from the contaminated Odiel and Tinto estuary in SW Spain. We studied the effect of cestodes on the response of Artemia to arsenic (acute toxicity tests, 24h LC50) and found that infection consistently reduced mortality across a range of arsenic concentrations. An increase from 25°C to 29°C, simulating the change in mean temperature expected under climate change, increased arsenic toxicity, but the benefits of infection persisted. Infected individuals showed higher levels of catalase and glutathione reductase activity, antioxidant enzymes with a very important role in the protection against oxidative stress. Levels of TBARS were unaffected by parasites, suggesting that infection is not associated with oxidative damage. Moreover, infected Artemia had a higher number of carotenoid-rich lipid droplets which may also protect the host through the "survival of the fattest" principle and the antioxidant potential of carotenoids. This study illustrates the need to consider the multi-stress context (contaminants and temperature increase) in which host-parasite interactions occur.

Enhancer Runaway and the Evolution of Diploid Gene Expression.

Evidence is mounting that the evolution of gene expression plays a major role in adaptation and speciation. Understanding the evolution of gene regulatory regions is indeed an essential step in linking genotypes and phenotypes and in understanding the molecular mechanisms underlying evolutionary change. The common view is that expression traits (protein folding, expression timing, tissue localization and concentration) are under natural selection at the individual level. Here, we use a theoretical approach to show that, in addition, in diploid organisms, enhancer strength (i.e., the ability of enhancers to activate transcription) may increase in a runaway process due to competition for expression between homologous enhancer alleles. These alleles may be viewed as self-promoting genetic elements, as they spread without conferring a benefit at the individual level. They gain a selective advantage by getting associated to better genetic backgrounds: deleterious mutations are more efficiently purged when linked to stronger enhancers. This process, which has been entirely overlooked so far, may help understand the observed overrepresentation of cis-acting regulatory changes in between-species phenotypic differences, and sheds a new light on investigating the contribution of gene expression evolution to adaptation.

Interactions between Genetic and Ecological Effects on the Evolution of Life Cycles.

Sexual reproduction leads to an alternation between haploid and diploid phases, whose relative length varies widely across taxa. Previous genetical models showed that diploid or haploid life cycles may be favored, depending on dominance interactions and on effective recombination rates. By contrast, niche differentiation between haploids and diploids may favor biphasic life cycles, in which development occurs in both phases. In this article, we explore the interplay between genetical and ecological factors, assuming that deleterious mutations affect the competitivity of individuals within their ecological niche and allowing different effects of mutations in haploids and diploids (including antagonistic selection). We show that selection on a modifier gene affecting the relative length of both phases can be decomposed into a direct selection term favoring the phase with the highest mean fitness (due to either ecological differences or differential effects of mutations) and an indirect selection term favoring the phase in which selection is more efficient. When deleterious alleles occur at many loci and in the presence of ecological differentiation between haploids and diploids, evolutionary branching often occurs and leads to the stable coexistence of alleles coding for haploid and diploid cycles, while temporal variations in niche sizes may stabilize biphasic cycles.

Relating fitness to long-term environmental variations in natura.

Quantifying links between ecological processes and adaptation dynamics in natura remains a crucial challenge. Many studies have documented the strength, form and direction of selection, and its variations in space and time, but only a few managed to link these variations to their proximal causes. This step is, however, crucial, if we are to understand how the variation in selective pressure affects adaptive allele dynamics in natural settings. We used data from a long-term survey (about 30 years) monitoring the adaptation to insecticides of Culex pipiens mosquitoes in Montpellier area (France), focusing on three resistance alleles of the Ester locus. We used a population genetics model taking temporal and spatial variations in selective pressure into account, to assess the quantitative relationships between variations in the proximal agent of selection (amounts of insecticide sprayed) and the fitness of resistance alleles. The response to variations in selective pressure was fast, and the alleles displayed different fitness-to-environment relationships: the analyses revealed that even slight changes in insecticide doses could induce changes in the strength and direction of selection, thus changing the fitness ranking of the adaptive alleles. They also revealed that selective pressures other than the insecticides used for mosquito control affected the resistance allele dynamics. These fitness-to-environment relationships, fast responses and continuous evolution limit our ability to predict the outcome of adaptive allele dynamics in a changing environment, but they clearly contribute to the maintenance of polymorphism in natural populations. Our study also emphasizes the necessity of long-term surveys in evolutionary ecology.

The ontogeny of tolerance curves: habitat quality vs. acclimation in a stressful environment.

Stressful environments affect life-history components of fitness through (i) instantaneous detrimental effects, (ii) historical (carry-over) effects and (iii) history-by-environment interactions, including acclimation effects. The relative contributions of these different responses to environmental stress are likely to change along life, but such ontogenic perspective is often overlooked in studies of tolerance curves, precluding a better understanding of the causes of costs of acclimation, and more generally of fitness in temporally fine-grained environments. We performed an experiment in the brine shrimp Artemia to disentangle these different contributions to environmental tolerance, and investigate how they unfold along life. We placed individuals from three clones of A. parthenogenetica over a range of salinities during a week, before transferring them to a (possibly) different salinity for the rest of their lives. We monitored individual survival at repeated intervals throughout life, instead of measuring survival or performance at a given point in time, as commonly done in acclimation experiments. We then designed a modified survival analysis model to estimate phase-specific hazard rates, accounting for the fact that individuals may share the same treatment for only part of their lives. Our approach allowed us to distinguish effects of salinity on (i) instantaneous mortality in each phase (habitat quality effects), (ii) mortality later in life (history effects) and (iii) their interaction. We showed clear effects of early salinity on late survival and interactions between effects of past and current environments on survival. Importantly, analysis of the ontogenetic dynamics of the tolerance curve reveals that acclimation affects different parts of the curve at different ages. Adopting a dynamical view of the ontogeny of tolerance curve should prove useful for understanding niche limits in temporally changing environments, where the full sequence of environments experienced by an individual determines its overall environmental tolerance, and how it changes throughout life.

Distributions of epistasis in microbes fit predictions from a fitness landscape model.

How do the fitness effects of several mutations combine? Despite its simplicity, this question is central to the understanding of multilocus evolution. Epistasis (the interaction between alleles at different loci), especially epistasis for fitness traits such as reproduction and survival, influences evolutionary predictions "almost whenever multilocus genetics matters". Yet very few models have sought to predict epistasis, and none has been empirically tested. Here we show that the distribution of epistasis can be predicted from the distribution of single mutation effects, based on a simple fitness landscape model. We show that this prediction closely matches the empirical measures of epistasis that have been obtained for Escherichia coli and the RNA virus vesicular stomatitis virus. Our results suggest that a simple fitness landscape model may be sufficient to quantitatively capture the complex nature of gene interactions. This model may offer a simple and widely applicable alternative to complex metabolic network models, in particular for making evolutionary predictions.

Niche Limits of Symbiotic Gut Microbiota Constrain the Salinity Tolerance of Brine Shrimp.

Symbiosis generally causes an expansion of the niche of each partner along the axis for which a service is mutually provided. However, for other axes, the niche can be restricted to the intersection of each partner's niche and can thus be constrained rather than expanded by mutualism. We explore this phenomenon using Artemia as a model system. This crustacean is able to survive at very high salinities but not at low salinities, although its hemolymph's salinity is close to freshwater. We hypothesized that this low-salinity paradox results from poor performance of its associated microbiota at low salinity. We showed that, in sterile conditions, Artemia had low survival at all salinities when algae were the only source of carbon. In contrast, survival was high at all salinities when fed with yeast. We also demonstrated that bacteria isolated from Artemia's gut reached higher densities at high salinities than at low salinities, including when grown on algae. Taken together, our results show that Artemia can survive at low salinities, but their gut microbiota, which are required for algae digestion, have reduced fitness. Widespread facultative symbiosis may thus be an important determinant of niche limits along axes not specific to the mutualistic interaction.

Why join groups? Lessons from parasite-manipulated Artemia.

Grouping behaviours (e.g. schooling, shoaling and swarming) are commonly explicated through adaptive hypotheses such as protection against predation, access to mates or improved foraging. However, the hypothesis that aggregation can result from manipulation by parasites to increase their transmission has never been demonstrated. We investigated this hypothesis using natural populations of two crustacean hosts (Artemia franciscana and Artemia parthenogenetica) infected with one cestode and two microsporidian parasites. We found that swarming propensity increased in cestode-infected hosts and that red colour intensity was higher in swarming compared with non-swarming infected hosts. These effects likely result in increased cestode transmission to its final avian host. Furthermore, we found that microsporidian-infected hosts had both increased swarming propensity and surfacing behaviour. Finally, we demonstrated using experimental infections that these concurrent manipulations result in increased spore transmission to new hosts. Hence, this study suggests that parasites can play a prominent role in host grouping behaviours.

Cytological, molecular and life cycle characterization of Anostracospora rigaudi n. g., n. sp. and Enterocytospora artemiae n. g., n. sp., two new microsporidian parasites infecting gut tissues of the brine shrimp Artemia.

Two new microsporidia, Anostracospora rigaudi n. g., n. sp., and Enterocytospora artemiae n. g., n. sp. infecting the intestinal epithelium of Artemia parthenogenetica Bowen and Sterling, 1978 and Artemia franciscana Kellogg, 1906 in southern France are described. Molecular analyses revealed the two species belong to a clade of microsporidian parasites that preferentially infect the intestinal epithelium of insect and crustacean hosts. These parasites are morphologically distinguishable from other gut microsporidia infecting Artemia. All life cycle stages have isolated nuclei. Fixed spores measure 1·3×0·7 µm with 5-6 polar tube coils for A. rigaudi and 1·2×0·9 µm with 4 polar tube coils for E. artemiae. Transmission of both species is horizontal, most likely through the ingestion of spores released with the faeces of infected hosts. The minute size of these species, together with their intestinal localization, makes their detection and identification difficult. We developed two species-specific molecular markers allowing each type of infection to be detected within 3-6 days post-inoculation. Using these markers, we show that the prevalence of these microsporidia ranges from 20% to 75% in natural populations. Hence, this study illustrates the usefulness of molecular approaches to study prevalent, but cryptic, infections involving microsporidian parasites of gut tissues.

No recombination suppression in asexually produced males of Daphnia pulex.

Obligate parthenogenesis (OP) is often thought to evolve by disruption of reductional meiosis and suppression of crossover recombination. In the crustacean Daphnia pulex, OP lineages, which have evolved from cyclical parthenogenetic (CP) ancestors, occasionally produce males that are capable of reductional meiosis. Here, by constructing high-density linkage maps, we find that these males show only slightly and nonsignificantly reduced recombination rates compared to CP males and females. Both meiosis disruption and recombination suppression are therefore sex-limited (or partly so), which speaks against the evolution of OP by disruption of a gene that is essential for meiosis or recombination in both sexes. The findings may be explained by female-limited action of genes that suppress recombination, but previously identified candidate genes are known to be expressed in both sexes. Alternatively, and equally consistent with the data, OP might have evolved through a reuse of the parthenogenesis pathways already present in CP and through their extension to all events of oogenesis. The causal mutations for the CP to OP transition may therefore include mutations in genes involved in oogenesis regulation and may not necessarily be restricted to genes of the "meiosis toolkit." More generally, our study emphasizes that there are many ways to achieve asexuality, and elucidating the possible mechanisms is key to ultimately identify the genes and traits involved.

Asexual male production by ZW recombination in Artemia parthenogenetica.

In some asexual species, parthenogenetic females occasionally produce males, which may strongly affect the evolution and maintenance of asexuality if they cross with related sexuals and transmit genes causing asexuality to their offspring ("contagious parthenogenesis"). How these males arise in the first place has remained enigmatic, especially in species with sex chromosomes. Here, we test the hypothesis that rare, asexually produced males of the crustacean Artemia parthenogenetica are produced by recombination between the Z and W sex chromosomes during non-clonal parthenogenesis, resulting in ZZ males through loss of heterozygosity at the sex determination locus. We used RAD-sequencing to compare asexual mothers with their male and female offspring. Markers on several sex-chromosome scaffolds indeed lost heterozygosity in all male but no female offspring, suggesting that they correspond to the sex-determining region. Other sex-chromosome scaffolds lost heterozygosity in only a part of the male offspring, consistent with recombination occurring at a variable location. Alternative hypotheses for the production of these males (such as partial or total hemizygosity of the Z) could be excluded. Rare males are thus produced because recombination is not entirely suppressed during parthenogenesis in A. parthenogenetica. This finding may contribute to explaining the maintenance of recombination in these asexuals.

Y recombination arrest and degeneration in the absence of sexual dimorphism.

Current theory proposes that degenerated sex chromosomes-such as the mammalian Y-evolve through three steps: (i) recombination arrest, linking male-beneficial alleles to the Y chromosome; (ii) Y degeneration, resulting from the inefficacy of selection in the absence of recombination; and (iii) dosage compensation, correcting the resulting low expression of X-linked genes in males. We investigate a model of sex chromosome evolution that incorporates the coevolution of cis and trans regulators of gene expression. We show that the early emergence of dosage compensation favors the maintenance of Y-linked inversions by creating sex-antagonistic regulatory effects. This is followed by degeneration of these nonrecombining inversions caused by regulatory divergence between the X and Y chromosomes. In contrast to current theory, the whole process occurs without any selective pressure related to sexual dimorphism.

Dosage compensation evolution in plants: theories, controversies and mechanisms.

In a minority of flowering plants, separate sexes are genetically determined by sex chromosomes. The Y chromosome has a non-recombining region that degenerates, causing a reduced expression of Y genes. In some species, the lower Y expression is accompanied by dosage compensation (DC), a mechanism that re-equalizes male and female expression and/or brings XY male expression back to its ancestral level. Here, we review work on DC in plants, which started as early as the late 1960s with cytological approaches. The use of transcriptomics fired a controversy as to whether DC existed in plants. Further work revealed that various plants exhibit partial DC, including a few species with young and homomorphic sex chromosomes. We are starting to understand the mechanisms responsible for DC in some plants, but in most species, we lack the data to differentiate between global and gene-by-gene DC. Also, it is unknown why some species evolve many dosage compensated genes while others do not. Finally, the forces that drive DC evolution remain mysterious, both in plants and animals. We review the multiple evolutionary theories that have been proposed to explain DC patterns in eukaryotes with XY or ZW sex chromosomes. This article is part of the theme issue 'Sex determination and sex chromosome evolution in land plants'.

Phenotypic but no genetic adaptation in zooplankton 24 years after an abrupt +10°C climate change.

The climate is currently warming fast, threatening biodiversity all over the globe. Populations often adapt rapidly to environmental change, but for climate warming very little evidence is available. Here, we investigate the pattern of adaptation to an extreme +10°C climate change in the wild, following the introduction of brine shrimp Artemia franciscana from San Francisco Bay, USA, to Vinh Chau saltern in Vietnam. We use a resurrection ecology approach, hatching diapause eggs from the ancestral population and the introduced population after 13 and 24 years (∼54 and ∼100 generations, respectively). In a series of coordinated experiments, we determined whether the introduced Artemia show increased tolerance to higher temperatures, and the extent to which genetic adaptation, developmental plasticity, transgenerational effects, and local microbiome differences contributed to this tolerance. We find that introduced brine shrimp do show increased phenotypic tolerance to warming. Yet strikingly, these changes do not have a detectable additive genetic component, are not caused by mitochondrial genetic variation, and do not seem to be caused by epigenetic marks set by adult parents exposed to warming. Further, we do not find any developmental plasticity that would help cope with warming, nor any protective effect of heat-tolerant local microbiota. The evolved thermal tolerance might therefore be entirely due to transgenerational (great)grandparental effects, possibly epigenetic marks set by parents who were exposed to high temperatures as juveniles. This study is a striking example of "missing heritability," where a large adaptive phenotypic change is not accompanied by additive genetic effects.

Distance-limited dispersal promotes coexistence at habitat boundaries: reconsidering the competitive exclusion principle.

Understanding the conditions for the stable coexistence of different alleles or species is a central topic in theoretical evolution and ecology. Different causes for stable polymorphism or species coexistence have already been identified but they can be grouped into a limited number of general processes. This article is devoted to the presentation and illustration of a new process, which we call 'habitat boundary polymorphism', and which relies on two key ingredients: habitat heterogeneity and distance-limited dispersal. Under direct competition and with fixed population densities, we show that this process allows for the equilibrium coexistence of more than n types in a n-habitat environment. Distance-limited dispersal indeed creates local maladaptation at habitat edges, which leaves room for the invasion of more generalist alleles or species. This mechanism provides a generic yet neglected process for the maintenance of polymorphism or species coexistence.