Species-level Selection Research Articles

Host genotype and exercise exhibit species-level selection for members of the gut bacterial communities in the mouse digestive system

The mammalian gut microbiome can potentially impact host health and disease state. It is known that the mouse-genome, eating-behavior, and exercise-status promotes higher taxonomic rank-level alterations (e.g. family to phyla-level) of the gut microbiota. Here, host genotype or activity status was investigated to determine if selection of individual bacterial species or strains could be discerned within the murine digestive system. For this study, the fecal bacterial community of adenylyl cyclase 5 knock-out (AC5KO, n = 7) mice or their wild-type (WT, n = 10) littermates under exercise or sedentary conditions were profiled by sequencing rRNA operons. AC5KO mice were chosen since this genotype displays enhanced longevity/exercise capacity and protects against cardiovascular/metabolic disease. Profiling of rRNA operons using the Oxford MinION yielded 65,706 2-D sequences (after size selection of 3.7–5.7 kb) which were screened against an NCBI 16S rRNA gene database. These sequences were binned into 1,566 different best BLAST hits (BBHs) and counted for each mouse sample. Non-metric multidimensional scaling (NMDS) of the gut microbial community demonstrated clustering by physical activity (p = 0.001) but not by host genotype. Additionally, sequence similarity and phylogenetic analysis demonstrated that different bacterial species (closely related to Muribaculum intestinale and Parasutterella excrementihominis) inhabit AC5KO or WT mice depending on activity status. Other bacterial species of the gut microbiota did not follow such patterning (e.g. Turicibacter sanguinis and Turicimonas muris). Our results support the need of improved taxonomic resolution for better characterization of bacterial communities to deepen our understanding of the role of the gut microbiome on host health.

Aging asexual lineages and the evolutionary maintenance of sex.

Finite populations of asexual and highly selfing species suffer from a reduced efficacy of selection. Such populations are thought to decline in fitness over time due to accumulating slightly deleterious mutations or failing to adapt to changing conditions. These within-population processes that lead nonrecombining species to extinction may help maintain sex and outcrossing through species level selection. Although inefficient selection is proposed to elevate extinction rates over time, previous models of species selection for sex assumed constant diversification rates. For sex to persist, classic models require that asexual species diversify at rates lower than sexual species; the validity of this requirement is questionable, both conceptually and empirically. We extend past models by allowing asexual lineages to decline in diversification rates as they age, that is nonrecombining lineages "senesce" in diversification rates. At equilibrium, senescing diversification rates maintain sex even when asexual lineages, at young ages, diversify faster than their sexual progenitors. In such cases, the age distribution of asexual lineages contains a peak at intermediate values rather than showing the exponential decline predicted by the classic model. Coexistence requires only that the average rate of diversification in asexuals be lower than that of sexuals.

Corolla morphology influences diversification rates in bifid toadflaxes (Linaria sect. Versicolores)

The role of flower specialization in plant speciation and evolution remains controversial. In this study the evolution of flower traits restricting access to pollinators was analysed in the bifid toadflaxes (Linaria sect. Versicolores), a monophyletic group of ~30 species and subspecies with highly specialized corollas. A time-calibrated phylogeny based on both nuclear and plastid DNA sequences was obtained using a coalescent-based method, and flower morphology was characterized by means of morphometric analyses. Directional trends in flower shape evolution and trait-dependent diversification rates were jointly analysed using recently developed methods, and morphological shifts were reconstructed along the phylogeny. Pollinator surveys were conducted for a representative sample of species. A restrictive character state (narrow corolla tube) was reconstructed in the most recent common ancestor of Linaria sect. Versicolores. After its early loss in the most species-rich clade, this character state has been convergently reacquired in multiple lineages of this clade in recent times, yet it seems to have exerted a negative influence on diversification rates. Comparative analyses and pollinator surveys suggest that the narrow- and broad-tubed flowers are evolutionary optima representing divergent strategies of pollen placement on nectar-feeding insects. The results confirm that different forms of floral specialization can lead to dissimilar evolutionary success in terms of diversification. It is additionally suggested that opposing individual-level and species-level selection pressures may have driven the evolution of pollinator-restrictive traits in bifid toadflaxes.

A geographic test of species selection using planktonic foraminifera during the Cretaceous/Paleogene mass extinction

Species selection has received a great deal of theoretical attention but it has rarely been empirically tested. It is important to determine the level of selection that operated during a particular extinction event because it can help distinguish between traits that were actually responsible for extinction and those that were merely correlated with it. Here, we present a test that can help distinguish between organismal and species-level selection, which we demonstrate using the high-resolution fossil record of planktonic foraminifera species recorded in deep-sea sediment cores. Our test examines the fate of survivors and victims during the Cretaceous/Paleogene (K/Pg) mass extinction within single geographic regions, where all individuals experience the same selection pressures. Selection at the organismal level implies that individual members of surviving species are more fit than those of victimized species, and therefore should be more likely to survive in affected areas; conversely, selection at the species level implies individuals will suffer equally within an affected area. We find that survivors of the mass extinction suffered very high extirpation rates in cores where the overall extinction rate was high, indicating that individual members of the surviving species were generally no more fit than individual members of extinct species. Rather, these species were able to survive because they possessed advantageous species-level traits, such as larger geographic ranges and greater abundances than victimized species. This geographic pattern of extirpation suggests that selection operated at the species, rather than organismal, level during the K/Pg mass extinction of planktonic foraminifera.

Species Selection Maintains Self-Incompatibility

Identifying traits that affect rates of speciation and extinction and, hence, explain differences in species diversity among clades is a major goal of evolutionary biology. Detecting such traits is especially difficult when they undergo frequent transitions between states. Self-incompatibility, the ability of hermaphrodites to enforce outcrossing, is frequently lost in flowering plants, enabling self-fertilization. We show, however, that in the nightshade plant family (Solanaceae), species with functional self-incompatibility diversify at a significantly higher rate than those without it. The apparent short-term advantages of potentially self-fertilizing individuals are therefore offset by strong species selection, which favors obligate outcrossing.

Orchid pollination by sexual deception: pollinator perspectives

The extraordinary taxonomic and morphological diversity of orchids is accompanied by a remarkable range of pollinators and pollination systems. Sexually deceptive orchids are adapted to attract specific male insects that are fooled into attempting to mate with orchid flowers and inadvertently acting as pollinators. This review summarises current knowledge, explores new hypotheses in the literature, and introduces some new approaches to understanding sexual deception from the perspective of the duped pollinator. Four main topics are addressed: (1) global patterns in sexual deception, (2) pollinator identities, mating systems and behaviours, (3) pollinator perception of orchid deceptive signals, and (4) the evolutionary implications of pollinator responses to orchid deception, including potential costs imposed on pollinators by orchids. A global list of known and putative sexually deceptive orchids and their pollinators is provided and methods for incorporating pollinator perspectives into sexual deception research are provided and reviewed. At present, almost all known sexually deceptive orchid taxa are from Australia or Europe. A few sexually deceptive species and genera are reported for New Zealand and South Africa. In Central and Southern America, Asia, and the Pacific many more species are likely to be identified in the future. Despite the great diversity of sexually deceptive orchid genera in Australia, pollination rates reported in the literature are similar between Australian and European species. The typical pollinator of a sexually deceptive orchid is a male insect of a species that is polygynous, monandrous, haplodiploid, and solitary rather than social. Insect behaviours involved in the pollination of sexually deceptive orchids include pre-copulatory gripping of flowers, brief entrapment, mating, and very rarely, ejaculation. Pollinator behaviour varies within and among pollinator species. Deception involving orchid mimicry of insect scent signals is becoming well understood for some species, but visual and tactile signals such as colour, shape, and texture remain neglected. Experimental manipulations that test for function, multi-signal interactions, and pollinator perception of these signals are required. Furthermore, other forms of deception such as exploitation of pollinator sensory biases or mating preferences merit more comprehensive investigation. Application of molecular techniques adapted from model plants and animals is likely to deliver new insights into orchid signalling, and pollinator perception and behaviour. There is little current evidence that sexual deception drives any species-level selection on pollinators. Pollinators do learn to avoid deceptive orchids and their locations, but this is not necessarily a response specific to orchids. Even in systems where evidence suggests that orchids do interfere with pollinator mating opportunities, considerable further research is required to determine whether this is sufficient to impose selection on pollinators or generate antagonistic coevolution or an arms race between orchids and their pollinators. Botanists, taxonomists and chemical ecologists have made remarkable progress in the study of deceptive orchid pollination. Further complementary investigations from entomology and behavioural ecology perspectives should prove fascinating and engender a more complete understanding of the evolution and maintenance of such enigmatic plant-animal interactions.

A Defense of Sociobiology

To counter recent claims that sociobiology is in disarray or requires reformulation, I discuss the semantics, theory, and data that underlie the field. A historical perspective is used to identify the cause of current debates. I argue that semantic precision is required in discussing terms such as kin selection, group selection, and altruism, but once care is taken, the objections to the unity of theoretical sociobiology largely evaporate. More work is required, however, to understand group adaptation, which might be taken to be the process of optimizing phenotypes that is driven by group, rather than individual, context. From the empirical perspective, the eusocial insects with their fixed division between work and reproduction are often a sounding board in discussions. Here, one finds clear evidence for the role of kin selection and relatedness in both the origin of eusociality and its maintenance. Data from other systems including the social vertebrates, microorganisms, and even plants also support the role of relatedness and particularly family life in the evolution of cooperation and altruism. These data, however, in no way invalidate the claim that group selection is also a central process in social evolution and I discuss the empirical evidence for group selection. The foundations of sociobiology are solid and the future should build on these foundations. Exciting new areas include the importance of community and species-level selection in evolution and elucidating the molecular mechanisms that underlie social traits.

Species‐level selection reduces selfishness through competitive exclusion

Adaptation does not necessarily lead to traits which are optimal for the population. This is because selection is often the strongest at the individual or gene level. The evolution of selfishness can lead to a 'tragedy of the commons', where traits such as aggression or social cheating reduce population size and may lead to extinction. This suggests that species-level selection will result whenever species differ in the incentive to be selfish. We explore this idea in a simple model that combines individual-level selection with ecology in two interacting species. Our model is not influenced by kin or trait-group selection. We find that individual selection in combination with competitive exclusion greatly increases the likelihood that selfish species go extinct. A simple example of this would be a vertebrate species that invests heavily into squabbles over breeding sites, which is then excluded by a species that invests more into direct reproduction. A multispecies simulation shows that these extinctions result in communities containing species that are much less selfish. Our results suggest that species-level selection and community dynamics play an important role in regulating the intensity of conflicts in natural populations.

On the heritability of geographic range sizes.

Within taxonomic groups, most species are restricted in their geographic range sizes, with only a few being widespread. The possibility that species-level selection on range sizes contributes to the characteristic form of such species-range size distributions has previously been raised. This would require that closely related species have similar range sizes, an indication of "heritability" of range sizes at the species level. Support for this view came from a positive correlation between the range sizes of closely related pairs of fossil mollusc species. We extend this analysis by considering the relationship between the geographic range sizes of 103 pairs of contemporary avian sister species. Range sizes in these sister species show no evidence of being more similar to each other than expected by chance. A reassessment of the mollusc data also suggests that the high correlation was probably overestimated because of the skewed nature of range size data. The fact that sister species tend to have similar life histories and ecologies suggests that any relationship between range sizes and biology is likely to be complicated and will be influenced by historical factors, such as mode of speciation and postspeciation range size transformations.

Sex Chromosome Meiotic Drive

▪ Abstract Sex chromosome drive refers to the unequal transmission of X and Y chromosomes from individuals of the heterogametic sex, resulting in biased sex ratios among progeny and within populations. The presence of driving sex chromosomes can reduce mean fitness within a population, bring about intragenomic conflict between the X chromosome, the Y, and the autosomes, and alter the intensity or mode of sexual selection within species. Sex chromosome drive, or its genetic equivalent, is known in plants, mammals, and flies. Many species harboring driving X chromosomes have evolved Y-linked and autosomal suppressors of drive. If a drive polymorphism is not stable, then driving chromosomes may spread to fixation and cause the extinction of a species. Certain characteristics of species, such as population density and female mating rate, may affect the probability of fixation of driving chromosomes. Thus, sex chromosome drive could be an agent of species-level selection.

Heritability at the Species Level: Analysis of Geographic Ranges of Cretaceous Mollusks

Geographic range has been regarded as a property of species rather than of individuals and thus as a potential factor in macroevolutionary processes. Species durations in Late Cretaceous mollusks exhibit statistically significant positive relationships with geographic range, and the attainment of a typical frequency distribution of geographic ranges in the cohort of species that originated just before the end-Cretaceous extinction indicates that species duration is the dependent variable. The strong relation between geographic ranges in pairs of closely related species indicates that the trait is, in effect, heritable at the species level. The significant heritabilities strengthen claims for processes of evolution by species-level selection, and for differential survivorship of organismic-level traits owing to extinction and origination processes operating at higher levels.