What cost mitochondria? The maintenance of functional mitochondrial DNA within and across generations

The peculiar biology of mitochondrial DNA (mtDNA) potentially has detrimental consequences for organismal health and lifespan. Typically, eukaryotic cells contain multiple mitochondria, each with multiple mtDNA genomes. The high copy number of mtDNA implies that selection on mtDNA functionality is relaxed. Furthermore, because mtDNA replication is not strictly regulated, within-cell selection may favour mtDNA variants with a replication advantage, but a deleterious effect on cell fitness. The opportunities for selfish mtDNA mutations to spread are restricted by various organism-level adaptations, such as uniparental transmission, germline mtDNA bottlenecks, germline selection and, during somatic growth, regular alternation between fusion and fission of mitochondria. These mechanisms are all hypothesized to maintain functional mtDNA. However, the strength of selection for maintenance of functional mtDNA progressively declines with age, resulting in age-related diseases. Furthermore, organismal adaptations that most probably evolved to restrict the opportunities for selfish mtDNA create secondary problems. Owing to predominantly maternal mtDNA transmission, recombination among mtDNA from different individuals is highly restricted or absent, reducing the scope for repair. Moreover, maternal inheritance precludes selection against mtDNA variants with male-specific effects. We finish by discussing the consequences of life-history differences among taxa with respect to mtDNA evolution and make a case for the use of microorganisms to experimentally manipulate levels of selection.     

Flies on the move: an inherited virus mirrors Drosophila melanogaster's elusive ecology and demography

Vertically transmitted parasites rely on their host's reproduction for their transmission, leading to the evolutionary histories of both parties being intimately entwined. Parasites can thus serve as a population genetic magnifying glass for their host's demographic history. Here, we study the fruitfly Drosophila melanogaster's vertically transmitted sigma virus DMelSV. The virus has a high mutation rate and low effective population size, allowing us to reconstruct at a fine scale how the combined forces of the movement of flies and selection on the virus have shaped its migration patterns. We found that the virus is likely to have spread to Europe from Africa, mirroring the colonization route of Drosophila. The North American DMelSV population appears to be the result of a recent single immigration from Europe, invading together with its host in the late 19th century. Across Europe, DMelSV migration rates are low and populations are highly genetically structured, likely reflecting limited fly movement. Despite being intolerant of extreme cold, viral diversity suggests that fly populations can persist in harsh continental climates and that recolonization from the warmer south plays a minor role. In conclusion, studying DMelSV can provide insights into the poorly understood ecology of D. melanogaster, one of the best‐studied organisms in biology.     

Pool and conquer: new tricks for (c)old problems

The early period of genetics is closely associated with the study of chromosomal inversions. For almost a century, evolutionary biologists found evidence for the role of inversions in central processes such as adaptation and speciation. In spite of huge efforts, many questions remain about the evolutionary forces underlying the distribution and dynamics of inversions in natural populations. Fortunately, old problems can be solved with new tools. In this issue, Kapun et al. ( 2014 ) present a remarkable combination of resources and techniques, including publicly available data, karyotyping, statistical estimation of haplotypes, Pool‐Seq data and experimental evolution, setting the ground for exciting developments in the field.     

Coalescence 2.0: a multiple branching of recent theoretical developments and their applications

Population genetics theory has laid the foundations for genomic analyses including the recent burst in genome scans for selection and statistical inference of past demographic events in many prokaryote, animal and plant species. Identifying SNPs under natural selection and underpinning species adaptation relies on disentangling the respective contribution of random processes (mutation, drift, migration) from that of selection on nucleotide variability. Most theory and statistical tests have been developed using the Kingman coalescent theory based on the Wright‐Fisher population model. However, these theoretical models rely on biological and life history assumptions which may be violated in many prokaryote, fungal, animal or plant species. Recent theoretical developments of the so‐called multiple merger coalescent models are reviewed here (Λ‐coalescent, beta‐coalescent, Bolthausen‐Sznitman, Ξ‐coalescent). We explain how these new models take into account various pervasive ecological and biological characteristics, life history traits or life cycles which were not accounted in previous theories such as (i) the skew in offspring production typical of marine species, (ii) fast adapting microparasites (virus, bacteria and fungi) exhibiting large variation in population sizes during epidemics, (iii) the peculiar life cycles of fungi and bacteria alternating sexual and asexual cycles and (iv) the high rates of extinction‐recolonization in spatially structured populations. We finally discuss the relevance of multiple merger models for the detection of SNPs under selection in these species, for population genomics of very large sample size and advocate to potentially examine the conclusion of previous population genetics studies.     

Ancient dates or accelerated rates? Morphological clocks and the antiquity of placental mammals

Analyses of a comprehensive morphological character matrix of mammals using ‘relaxed’ clock models (which simultaneously estimate topology, divergence dates and evolutionary rates), either alone or in combination with an 8.5 kb nuclear sequence dataset, retrieve implausibly ancient, Late Jurassic–Early Cretaceous estimates for the initial diversification of Placentalia (crown-group Eutheria). These dates are much older than all recent molecular and palaeontological estimates. They are recovered using two very different clock models, and regardless of whether the tree topology is freely estimated or constrained using scaffolds to match the current consensus placental phylogeny. This raises the possibility that divergence dates have been overestimated in previous analyses that have applied such clock models to morphological and total evidence datasets. Enforcing additional age constraints on selected internal divergences results in only a slight reduction of the age of Placentalia. Constraining Placentalia to less than 93.8 Ma, congruent with recent molecular estimates, does not require major changes in morphological or molecular evolutionary rates. Even constraining Placentalia to less than 66 Ma to match the ‘explosive’ palaeontological model results in only a 10- to 20-fold increase in maximum evolutionary rate for morphology, and fivefold for molecules. The large discrepancies between clock- and fossil-based estimates for divergence dates might therefore be attributable to relatively small changes in evolutionary rates through time, although other explanations (such as overly simplistic models of morphological evolution) need to be investigated. Conversely, dates inferred using relaxed clock models (especially with discrete morphological data and MrBayes) should be treated cautiously, as relatively minor deviations in rate patterns can generate large effects on estimated divergence dates.     

Sexually transmitted infection and the evolution of serial monogamy

The selective forces shaping mating systems have long been of interest to biologists. One particular selective pressure that has received comparatively little attention is sexually transmitted infections (STIs). While it has been hypothesized that STIs could drive the evolutionary emergence of monogamy, there is little theoretical support. Here we use an evolutionary invasion analysis to determine what aspects of pathogen virulence and transmission are necessary for serial monogamy to evolve in a promiscuous population. We derive a biologically intuitive invasion condition in terms of population-specific quantities. From this condition, we obtain two main results. First, when pathogen virulence causes mortality rather than sterility, monogamy is more likely to evolve. Second, we find that at intermediate pathogen transmission rates, monogamy is the most selectively advantageous, whereas at high- and low-transmission rates, monogamy is generally selected against. As a result, it is possible for a pathogen to be highly virulent, yet for promiscuity to persist.     

Mainstreaming Caenorhabditis elegans in experimental evolution

Experimental evolution provides a powerful manipulative tool for probing evolutionary process and mechanism. As this approach to hypothesis testing has taken purchase in biology, so too has the number of experimental systems that use it, each with its own unique strengths and weaknesses. The depth of biological knowledge about Caenorhabditis nematodes, combined with their laboratory tractability, positions them well for exploiting experimental evolution in animal systems to understand deep questions in evolution and ecology, as well as in molecular genetics and systems biology. To date, Caenorhabditis elegans and related species have proved themselves in experimental evolution studies of the process of mutation, host–pathogen coevolution, mating system evolution and life-history theory. Yet these organisms are not broadly recognized for their utility for evolution experiments and remain underexploited. Here, we outline this experimental evolution work undertaken so far in Caenorhabditis, detail simple methodological tricks that can be exploited and identify research areas that are ripe for future discovery.     

Low ecological disparity in Early Cretaceous birds

Ecological divergence is thought to be coupled with evolutionary radiations, yet the strength of this coupling is unclear. When birds diversified ecologically has received much less attention than their hotly debated crown divergence time. Here, we quantify how accurately skeletal morphology can predict ecology in living and extinct birds, and show that the earliest known assemblage of birds (= pygostylians) from the Jehol Biota (≈ 125 Ma) was substantially impoverished ecologically. The Jehol avifauna has few representatives of highly preservable ecomorphs (e.g. aquatic forms) and a notable lack of ecomorphological overlap with the pterosaur assemblage (e.g. no large or aerially foraging pygostylians). Comparisons of the Jehol functional diversity with modern and subfossil avian assemblages show that taphonomic bias alone cannot explain the ecomorphological impoverishment. However, evolutionary simulations suggest that the constrained ecological diversity of the Early Cretaceous pygostylians is consistent with what is expected from a relatively young radiation. Regardless of the proximate biological explanation, the anomalously low functional diversity of the Jehol birds is evidence both for ecological vacancies in Cretaceous ecosystems, which were subsequently filled by the radiation of crown Aves, and for discordance between taxonomic richness and ecological diversity in the best-known Mesozoic ecosystem.     

The genetic covariance between life cycle stages separated by metamorphosis

Metamorphosis is common in animals, yet the genetic associations between life cycle stages are poorly understood. Given the radical changes that occur at metamorphosis, selection may differ before and after metamorphosis, and the extent that genetic associations between pre- and post-metamorphic traits constrain evolutionary change is a subject of considerable interest. In some instances, metamorphosis may allow the genetic decoupling of life cycle stages, whereas in others, metamorphosis could allow complementary responses to selection across the life cycle. Using a diallel breeding design, we measured viability at four ontogenetic stages (embryo, larval, juvenile and adult viability), in the ascidian Ciona intestinalis and examined the orientation of additive genetic variation with respect to the metamorphic boundary. We found support for one eigenvector of G (g_obsmax), which contrasted larval viability against embryo viability and juvenile viability. Target matrix rotation confirmed that while g_obsmax shows genetic associations can extend beyond metamorphosis, there is still considerable scope for decoupled phenotypic evolution. Therefore, although genetic associations across metamorphosis could limit that range of phenotypes that are attainable, traits on either side of the metamorphic boundary are capable of some independent evolutionary change in response to the divergent conditions encountered during each life cycle stage.     

Experimental evidence for friction-enhancing integumentary modifications of chameleons and associated functional and evolutionary implications

The striking morphological convergence of hair-like integumentary derivatives of lizards and arthropods (spiders and insects) demonstrates the importance of such features for enhancing purchase on the locomotor substrate. These pilose structures are responsible for the unique tractive abilities of these groups of animals, enabling them to move with seeming ease on overhanging and inverted surfaces, and to traverse inclined smooth substrates. Three groups of lizards are well known for bearing adhesion-promoting setae on their digits: geckos, anoles and skinks. Similar features are also found on the ventral subdigital and distal caudal skin of chameleons. These have only recently been described in any detail, and structurally and functionally are much less well understood than are the setae of geckos and anoles. The seta-like structures of chameleons are not branched (a characteristic of many geckos), nor do they terminate in spatulate tips (which is characteristic of geckos, anoles and skinks). They are densely packed and have attenuated blunt, globose tips or broad, blade-like shafts that are flattened for much of their length. Using a force transducer, we tested the hypothesis that these structures enhance friction and demonstrate that the pilose skin has a greater frictional coefficient than does the smooth skin of these animals. Our results are consistent with friction being generated as a result of side contact of the integumentary filaments. We discuss the evolutionary and functional implications of these seta-like structures in comparison with those typical of other lizard groups and with the properties of seta-mimicking synthetic structures.