The language of isolation: a commentary on Westram et al., 2022

Good communication needs a common language. As Harrison (2012) pointed out, the ‘language of speciation’ has a complex evolutionary history, sometimes resulting in both modification and diversification in the use of terms. There is a risk that this erodes the effective exchange of ideas. It is surprising that Harrison did not discuss the meaning of ‘reproductive isolation’. He seems to have assumed, along with many others, that there is a common understanding of this term. In fact, it is not an easy term to define and the conversation started here by Westram et al. (2022) is both valuable and timely. Multiple terms are in use to describe the extent to which populations are connected by interbreeding and gene flow: ‘reproductive isolation’ itself, various terms for ‘components of reproductive isolation’ in a temporal sequence derived from Dobzhansky's seminal table (Dobzhansky, 1937, pp. 231– 232; prezygotic isolation, postzygotic isolation and a series of finer divisions), a partly independent categorization into ‘intrinsic’ vs ‘extrinsic’ components and a set of terms related to ‘barriers to gene flow’, such as ‘barrier traits’, ‘barrier loci’ and ‘barrier effects’. Having multiple terms is potentially confusing, but it can also be very helpful: if these terms have clear and distinct meanings, they can be used to make descriptions more precise and so to communicate more reliably. They can also guide decisions about what to measure empirically and help to show how different types of empirical information fit together. Westram et al. (2022) define ‘reproductive isolation’ as a quantitative measure of the effect that genetic differences between populations have on gene flow, specifically aiming to bring together what they describe as the ‘organismal focus’ and the ‘genetic focus’ revealed in their survey of practitioners. Here, I argue that better communication can be achieved by using the available terminology to describe different aspects of the evolutionary independence of populations rather than finding a single definition of reproductive isolation that incorporates all aspects. The issue of interest is the evolutionary independence of populations. This depends on gene flow, which tends to homogenize neutral variation, restrict responses to divergent selection and facilitate shared responses to common selection pressures. Populations of the same species have high levels of interdependence, whereas populations of different species can evolve independently (in a genetic sense: their evolutionary trajectories may well be constrained by ecological factors, but that is not the point at issue here). At this conceptual level, there is broad agreement and ‘reproductive isolation’ is used in a general sense to describe a continuum of relationships (Stankowski & Ravinet, 2021). The problems arise when trying to be more precise, especially when looking for quantitative comparisons. One key distinction to consider lies in the entities for which a quantitative measure is required. Reproductive isolation is generally considered a property of a pair of populations, but gene flow is only meaningful at the level of genes. In a theoretical construct of two populations connected by gene flow but experiencing no selection, it might be true that all loci have the same expected gene flow. However, such pairs of populations do not exist in nature. Habitat variation is ubiquitous, leading to divergent selection on a subset of loci and so lower gene flow for these loci. Even in the absence of divergent selection, gene flow would be expected to vary due to beneficial and deleterious mutations appearing independently in the two populations. Gene flow at neutral loci is influenced by linkage to