The chastity of amoebae: re-evaluating evidence for sex in amoeboid organisms

Amoebae are generally assumed to be asexual. We argue that this view is a relict of early classification schemes that lumped all amoebae together inside the 'lower' protozoa, separated from the 'higher' plants, animals and fungi. This artificial classification allowed microbial eukaryotes, including amoebae, to be dismissed as primitive, and implied that the biological rules and theories developed for macro-organisms need not apply to microbes. Eukaryotic diversity is made up of 70+ lineages, most of which are microbial. Plants, animals and fungi are nested among these microbial lineages. Thus, theories on the prevalence and maintenance of sex developed for macro-organisms should in fact apply to microbial eukaryotes, though the theories may need to be refined and generalized (e.g. to account for the variation in sexual strategies and prevalence of facultative sex in natural populations of many microbial eukaryotes). We use a revised phylogenetic framework to assess evidence for sex in several amoeboid lineages that are traditionally considered asexual, and we interpret this evidence in light of theories on the evolution of sex developed for macro-organisms. We emphasize that the limited data available for many lineages coupled with natural variation in microbial life cycles overestimate the extent of asexuality. Mapping sexuality onto the eukaryotic tree of life demonstrates that the majority of amoeboid lineages are, contrary to popular belief, anciently sexual, and that most asexual groups have probably arisen recently and independently. Additionally, several unusual genomic traits are prevalent in amoeboid lineages, including cyclic polyploidy, which may serve as alternative mechanisms to minimize the deleterious effects of asexuality.     

Evolutionary traction: the cost of adaptation and the evolution of sex

The advantage of sexual reproduction remains a puzzle for evolutionary biologists. Everything else being equal, asexual populations are expected to have twice the number of offspring produced by similar sexual populations. Yet, asexual species are uncommon among higher eukaryotes. In models assuming small populations, high mutation rates, or frequent environmental changes, sexual reproduction seems to have at least a two-fold advantage over asexuality. But the advantage of sex for large populations, low mutation rates, and rare or mild environmental changes remains a conundrum. Here we show that without recombination, rare advantageous mutations can result in increased accumulation of deleterious mutations ('evolutionary traction'), which explains the long-term advantage of sex under a wide parameter range.     

Evolution of polygenic traits under global vs local adaptation

Observations about the number, frequency, effect size, and genomic distribution of alleles associated with complex traits must be interpreted in light of evolutionary process. These characteristics, which constitute a trait’s genetic architecture, can dramatically affect evolutionary outcomes in applications from agriculture to medicine, and can provide a window into how evolution works. Here, I review theoretical predictions about the evolution of genetic architecture under spatially homogeneous, global adaptation as compared with spatially heterogeneous, local adaptation. Due to the tension between divergent selection and migration, local adaptation can favor “concentrated” genetic architectures that are enriched for alleles of larger effect, clustered in a smaller number of genomic regions, relative to expectations under global adaptation. However, the evolution of such architectures may be limited by many factors, including the genotypic redundancy of the trait, mutation rate, and temporal variability of environment. I review the circumstances in which predictions differ for global vs local adaptation and discuss where progress can be made in testing hypotheses using data from natural populations and lab experiments. As the field of comparative population genomics expands in scope, differences in architecture among traits and species will provide insights into how evolution works, and such differences must be interpreted in light of which kind of selection has been operating.     

Evolutionary adaptation to environmental pH in experimental lineages of Escherichia coli

This study uses the enteric bacterium Escherichia coli as an experimental system to examine evolutionary responses of bacteria to an environmental acidic-alkaline range between pH 5.3 and 7.8 (15-5000 nM [H(+)]). Our goal was both to test general hypotheses about adaptation to abiotic variables and to provide insights into how coliform organisms might respond to changing conditions inside and outside of hosts. Six replicate lines of E. coli evolved for 2000 generations at one of four different constant pH conditions: pH 5.3, 6.3, 7.0, or 7.8. Direct adaptation to the evolutionary environment, as well as correlated changes in other environments, was measured as a change in fitness relative to the ancestor in direct competition experiments. The pH 5.3 group had the highest fitness gains, with a highly significant increase of 20%. The pH 7.8 group had far less significant gains and much higher variance among its lines. Analysis of individual lines within these two groups revealed complex patterns of adaptation: all of the pH 5.3 lines exhibited trade-offs (reduced fitness in another environment), but only 33% of the pH 7.8 lines showed such trade-offs and one of the pH 7.8 lines demonstrated exaptation by improving fitness in the pH 5.3 environment. Although there was also prevalent exaptation in other groups to the acidic environment, there were no such cases of exaptation to alkalinity. Comparison across the entire experimental pH range revealed that the most acidic lines, the pH 5.3 group, were all specialists, in contrast to the pH 6.3 lines, which were almost all generalists. That is, although none of the pH 5.3 lines showed any correlated fitness gains, all of the pH 6.3 lines did.     

Sex is not a solution for reproduction: the libertine bubble theory

Here, I propose a new hypothesis: sex originated from an archaic gene transfer process among prebiotic bubbles without the prerequisite for reproduction. This de‐coupling from reproduction might make the thorny problem of accounting for the evolution of sex, despite the apparent advantages of parthenogenicity, more tractable.     

Triangulating the genetic basis of adaptation to multifarious selection

Understanding how natural populations adapt to their local environments is a major research theme for ecological genomics. This endeavour begins by sleuthing for shared genetic similarities among unrelated natural populations sharing adaptive traits to documented selective pressures. When the selective pressures have low dimensionality, and the genetic response is localized to a few genes of major effect, this detective work is relatively straightforward. However, in the real world, populations face a complex mixture of selective pressures and many adaptive responses are the result of changes in quantitative traits that have a polygenic genetic basis. This complex relationship between environment and adaptation presents a significant challenge. How can we begin to identify drivers of adaptation in natural settings? In this issue of Molecular Ecology, Orsini et al. (2012) take advantage of the biological attributes of the freshwater microcrustacean Daphnia ( Fig. 1 ) to disentangle multidimensional selection’s signature on the genome of populations that have repeatedly evolved adaptive responses to isolated selective pressures including predation, parasitism and anthropogenic changes in land use. Orsini et al. (2012) leverage a powerful combination of spatially structured populations in a geographic mosaic of environmental stressors, the historical archive of past genotypes preserved in lake‐bottom sediments and selection experiments to identify sets of candidate genomic regions associated with adaptation in response to these three environmental stressors. This study provides a template for future investigation in ecological genomics, combining multiple experimental approaches with the genomic investigation of a well‐studied ecological model species.

Figure 1 Open in figure viewer PowerPoint Adult Daphnia magna carrying a resting egg in the brood pouch. The water flea Daphnia is a renowned ecological model system and rapidly developing as an ecological and environmental genomics model species. Photo credit Joachim Mergeay.     

Meiotic recombination mirrors patterns of germline replication in mice and humans

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Chromosome Fusion Affects Genetic Diversity and Evolutionary Turnover of Functional Loci but Consistently Depends on Chromosome Size

Major changes in chromosome number and structure are linked to a series of evolutionary phenomena, including intrinsic barriers to gene flow or suppression of recombination due to chromosomal rearrangements. However, chromosome rearrangements can also affect the fundamental dynamics of molecular evolution within populations by changing relationships between linked loci and altering rates of recombination. Here, we build chromosome-level assembly Eueides isabella and, together with a recent chromosome-level assembly of Dryas iulia, examine the evolutionary consequences of multiple chromosome fusions in Heliconius butterflies. These assemblies pinpoint fusion points on 10 of the 20 autosomal chromosomes and reveal striking differences in the characteristics of fused and unfused chromosomes. The ten smallest autosomes in D. iulia and E. isabella, which have each fused to a longer chromosome in Heliconius, have higher repeat and GC content, and longer introns than predicted by their chromosome length. When fused, these characteristics change to become more in line with chromosome length. The fusions also led to reduced diversity, which likely reflects increased background selection and selection against introgression between diverging populations, following a reduction in per-base recombination rate. We further show that chromosome size and fusion impact turnover rates of functional loci at a macroevolutionary scale. Together these results provide further evidence that chromosome fusion in Heliconius likely had dramatic effects on population level processes shaping rates of neutral and adaptive divergence. These effects may have impacted patterns of diversification in Heliconius, a classic example of an adaptive radiation.     

Genome-wide variation in the human and fruitfly: a comparison

Average levels of nucleotide diversity are ten-fold lower in humans than in the fruitfly, Drosophila melanogaster. Despite this difference, apparently as a result of a lower population size, patterns of genomic diversity are strikingly similar in being correlated with local rates of recombination, and influenced by similar interactions between positive natural selection and recombination. Both species also show lower levels of variation on average in non-African compared to African populations, reflecting a similar evolutionary history and perhaps both natural selection and founder effects in new environments.     

The origin and evolution of sex chromosomes,revealed by sequencing of the Silene latifolia female genome

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Parallel genotypic adaptation: when evolution repeats itself

Until recently, parallel genotypic adaptation was considered unlikely because phenotypic differences were thought to be controlled by many genes. There is increasing evidence, however, that phenotypic variation sometimes has a simple genetic basis and that parallel adaptation at the genotypic level may be more frequent than previously believed. Here, we review evidence for parallel genotypic adaptation derived from a survey of the experimental evolution, phylogenetic, and quantitative genetic literature. The most convincing evidence of parallel genotypic adaptation comes from artificial selection experiments involving microbial populations. In some experiments, up to half of the nucleotide substitutions found in independent lineages under uniform selection are the same. Phylogenetic studies provide a means for studying parallel genotypic adaptation in non-experimental systems, but conclusive evidence may be difficult to obtain because homoplasy can arise for other reasons. Nonetheless, phylogenetic approaches have provided evidence of parallel genotypic adaptation across all taxonomic levels, not just microbes. Quantitative genetic approaches also suggest parallel genotypic evolution across both closely and distantly related taxa, but it is important to note that this approach cannot distinguish between parallel changes at homologous loci versus convergent changes at closely linked non-homologous loci. The finding that parallel genotypic adaptation appears to be frequent and occurs at all taxonomic levels has important implications for phylogenetic and evolutionary studies. With respect to phylogenetic analyses, parallel genotypic changes, if common, may result in faulty estimates of phylogenetic relationships. From an evolutionary perspective, the occurrence of parallel genotypic adaptation provides increasing support for determinism in evolution and may provide a partial explanation for how species with low levels of gene flow are held together.     

Responsible RAD: Striving for best practices in population genomic studies of adaptation

Two recent articles were written in response to our paper “Breaking RAD: An evaluation of the utility of restriction site associated DNA sequencing scans of adaptation.” While we agree with some of the comments made by the authors of these two response papers, we still believe caution should be employed in RADseq studies that aim to detect loci that contribute to adaptation. In this rebuttal, we evaluate the key points made in these papers, attempt to identify a middle ground and make suggestions for responsibly conducting future studies to understand the genomewide mechanisms of adaptation.     

Evolutionary plasticity in prokaryotes: A panglossian view

Enzyme directed genetic mechanisms causing random DNA sequence alterations are ubiquitous in both eukaryotes and prokaryotes. A number of molecular geneticist have invoked adaptation through natural selection to account for this fact, however, alternative explanations have also flourished. The population geneticist G.C. Williams has dismissed the possibility of selection for mutator activity on a priori grounds. In this paper, I attempt a refutation of Williams' argument. In addition, I discuss some conceptual problems related to recent claims made by microbiologists on the adaptiveness of molecular variety generators in the evolution of prokaryotes. A distinction is proposed between selection for mutations caused by a mutator activity and selection for the mutator activity proper. The latter requires a concept of fitness different from the one commonly used in microbiology.     

How plants conquered land: evolution of terrestrial adaptation

The transition of plants from water to land is considered one of the most significant events in the evolution of life on Earth. The colonization of land by plants, accompanied by their morphological, physiological and developmental changes, resulted in plant biodiversity. Besides significantly influencing oxygen levels in the air and on land, plants manufacture organic matter from CO₂ and water with the help of sunlight, paving the way for the diversification of nonplant lineages ranging from microscopic organisms to animals. Land plants regulate the climate by adjusting total biomass and energy flow. At the genetic level, these innovations are achieved through the rearrangement of pre-existing genetic information. Advances in genome sequencing technology are revamping our understanding of plant evolution. This study highlights the morphological and genomic innovations that allow plants to integrate life on Earth.     

Recombination and loss of complementation: a more than two-fold cost for parthenogenesis

Certain types of asexual reproduction lead to loss of complementation, that is unmasking of recessive deleterious alleles. A theoretical measure of this loss is calculated for apomixis, automixis and endomitosis in the cases of diploidy and polyploidy. The effect of the consequent unmasking of deleterious recessive mutations on fitness is also calculated. Results show that, depending on the number of lethal equivalents and on the frequency of recombination, the cost produced by loss of complementation after few generations of asexual reproduction may be greater than the two-fold cost of meiosis. Maintaining complementation may, therefore, provide a general short-term advantage for sexual reproduction. Apomixis can replace sexual reproduction under a wide range of parameters only if it is associated with triploidy or tetraploidy, which is consistent with our knowledge of the distribution of apomixis.     

Evolutionary history of a complex adaptation: Tetrodotoxin resistance in salamanders

Understanding the processes that generate novel adaptive phenotypes is central to evolutionary biology. We used comparative analyses to reveal the history of tetrodotoxin (TTX) resistance in TTX-bearing salamanders. Resistance to TTX is a critical component of the ability to use TTX defensively but the origin of the TTX-bearing phenotype is unclear. Skeletal muscle of TTX-bearing salamanders (modern newts, family: Salamandridae) is unaffected by TTX at doses far in excess of those that block action potentials in muscle and nerve of other vertebrates. Skeletal muscle of non-TTX-bearing salamandrids is also resistant to TTX but at lower levels. Skeletal muscle TTX resistance in the Salamandridae results from the expression of TTX-resistant variants of the voltage-gated sodium channel Na_V 1.4 (SCN4a). We identified four substitutions in the coding region of salSCN4a that are likely responsible for the TTX resistance measured in TTX-bearing salamanders and variation at one of these sites likely explains variation in TTX resistance among other lineages. Our results suggest that exaptation has played a role in the evolution of the TTX-bearing phenotype and provide empirical evidence that complex physiological adaptations can arise through the accumulation of beneficial mutations in the coding region of conserved proteins.     

Evolutionary responses to environmental change: trophic interactions affect adaptation and persistence

According to recent reviews, the question of how trophic interactions may affect evolutionary responses to climate change remains unanswered. In this modelling study, we explore the evolutionary dynamics of thermal and plant–herbivore interaction traits in a warming environment. We find the herbivore usually reduces adaptation speed and persistence time of the plant by reducing biomass. However, if the plant interaction trait and thermal trait are correlated, herbivores can create different coevolutionary attractors. One attractor has a warmer plant thermal optimum, and the other a colder one compared with the environment. A warmer plant thermal strategy is given a head start under warming, the only case where herbivores can increase plant persistence under warming. Persistence time of the plant under warming is maximal at small or large thermal niche width. This study shows that considering trophic interactions is necessary and feasible for understanding how ecosystems respond to climate change.