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Speciation is often viewed as a continuum along which populations diverge until they become reproductively-isolated species. However, such divergence may be heterogeneous, proceeding in fits and bursts, rather than being uniform and gradual. We show inTimemastick insects that one component of reproductive isolation evolves non-uniformly across this continuum, whereas another does not. Specifically, we use thousands of host-preference and mating trials to study habitat and sexual isolation among 42 pairs of taxa spanning a range of genomic differentiation and divergence time. We find that habitat isolation is uncoupled from genomic differentiation within species, but accumulates linearly with it between species. In contrast, sexual isolation accumulates linearly across the speciation continuum, and thus exhibits similar dynamics to morphological traits not implicated in reproductive isolation. The results show different evolutionary dynamics for different components of reproductive isolation and highlight a special relevance for species status in the process of speciation.

 

Genome re-arrangements such as chromosomal inversions are often involved in adaptation. As such, they experience natural selection, which can erode genetic variation. Thus, whether and how inversions can remain polymorphic for extended periods of time remains debated. Here we combine genomics, experiments, and evolutionary modeling to elucidate the processes maintaining an inversion polymorphism associated with the use of a challenging host plant (Redwood trees) inTimemastick insects. We show that the inversion is maintained by a combination of processes, finding roles for life-history trade-offs, heterozygote advantage, local adaptation to different hosts, and gene flow. We use models to show how such multi-layered regimes of balancing selection and gene flow provide resilience to help buffer populations against the loss of genetic variation, maintaining the potential for future evolution. We further show that the inversion polymorphism has persisted for millions of years and is not a result of recent introgression. We thus find that rather than being a nuisance, the complex interplay of evolutionary processes provides a mechanism for the long-term maintenance of genetic variation.

 

There is increasing evidence that genetic evolution can occur rapidly enough to affect the ecological dynamics of populations and communities ( 1 – 3 ). To better predict the future of ecosystems, it is necessary to understand how evolutionary changes within species influence and interact with ecological changes through processes known as “eco-evolutionary dynamics” ( 4 ). On page 70 of this issue, Barbour et al. ( 5 ) demonstrate that a gene affecting a plant’s resistance to herbivory also influences the persistence of the food web through the gene’s effect on plant growth (see the figure). Subsequent studies of natural selection in the wild can help explain how variations of such “keystone genes” can be maintained ( 6 , 7 ). The maintenance of genetic variation in keystone genes is required for eco-evolutionary dynamics to be perpetual rather than transient. 

Identifying the genetic basis of adaptation is a central goal of evolutionary biology. However, identifying genes and mutations affecting fitness remains challenging because a large number of traits and variants can influence fitness. Selected phenotypes can also be difficult to know a priori , complicating top–down genetic approaches for trait mapping that involve crosses or genome-wide association studies. In such cases, experimental genetic approaches, where one maps fitness directly and attempts to infer the traits involved afterwards, can be valuable. Here, we re-analyse data from a transplant experiment involving Timema stick insects, where five physically clustered single-nucleotide polymorphisms associated with cryptic body coloration were shown to interact to affect survival. Our analysis covers a larger genomic region than past work and revealed a locus previously not identified as associated with survival. This locus resides near a gene, Punch ( Pu ) , involved in pteridine pigments production, implying that it could be associated with an unmeasured coloration trait. However, by combining previous and newly obtained phenotypic data, we show that this trait is not eye or body coloration. We discuss the implications of our results for the discovery of traits, genes and mutations associated with fitness in other systems, as well as for supergene evolution. This article is part of the theme issue ‘Genetic basis of adaptation and speciation: from loci to causative mutations’. 

Our ability to predict natural phenomena can be limited by incomplete information. This issue is exemplified by `Laplace's demon', an imaginary creature proposed in the 18th century, who knew everything about everything, and thus could predict the full nature of the universe forward or backward in time. Quantum mechanics, among other things, has cast doubt on the possibility of Laplace's demon in the full sense, but the idea still serves as a useful metaphor for thinking about the extent to which prediction is limited by incomplete information on deterministic processes versus random factors. Here we use simple analytical models and computer simulations to illustrate how data limits can be captured in a Bayesian framework, and how they influence our ability to predict evolution. We show how uncertainty in measurements of natural selection, or low predictability of external environmental factors affecting selection, can greatly reduce predictive power, often swamping the influence of intrinsic randomness caused by genetic drift. Thus, more accurate knowledge concerning the causes and action of natural selection is key to improving prediction. Fortunately, our analyses and simulations show quantitatively that reasonable improvements in data quantity and quality can meaningfully increase predictability.