TY - JOUR AB - Local adaptation leads to differences between populations within a species. In many systems, similar environmental contrasts occur repeatedly, sometimes driving parallel phenotypic evolution. Understanding the genomic basis of local adaptation and parallel evolution is a major goal of evolutionary genomics. It is now known that by preventing the break-up of favourable combinations of alleles across multiple loci, genetic architectures that reduce recombination, like chromosomal inversions, can make an important contribution to local adaptation. However, little is known about whether inversions also contribute disproportionately to parallel evolution. Our aim here is to highlight this knowledge gap, to showcase existing studies, and to illustrate the differences between genomic architectures with and without inversions using simple models. We predict that by generating stronger effective selection, inversions can sometimes speed up the parallel adaptive process or enable parallel adaptation where it would be impossible otherwise, but this is highly dependent on the spatial setting. We highlight that further empirical work is needed, in particular to cover a broader taxonomic range and to understand the relative importance of inversions compared to genomic regions without inversions. AU - Westram, Anja M AU - Faria, Rui AU - Johannesson, Kerstin AU - Butlin, Roger AU - Barton, Nicholas H ID - 11546 IS - 1856 JF - Philosophical Transactions of the Royal Society B: Biological Sciences KW - General Agricultural and Biological Sciences KW - General Biochemistry KW - Genetics and Molecular Biology SN - 0962-8436 TI - Inversions and parallel evolution VL - 377 ER - TY - JOUR AB - A species distributed across diverse environments may adapt to local conditions. We ask how quickly such a species changes its range in response to changed conditions. Szép et al. (Szép E, Sachdeva H, Barton NH. 2021 Polygenic local adaptation in metapopulations: a stochastic eco-evolutionary model. Evolution75, 1030–1045 (doi:10.1111/evo.14210)) used the infinite island model to find the stationary distribution of allele frequencies and deme sizes. We extend this to find how a metapopulation responds to changes in carrying capacity, selection strength, or migration rate when deme sizes are fixed. We further develop a ‘fixed-state’ approximation. Under this approximation, polymorphism is only possible for a narrow range of habitat proportions when selection is weak compared to drift, but for a much wider range otherwise. When rates of selection or migration relative to drift change in a single deme of the metapopulation, the population takes a time of order m−1 to reach the new equilibrium. However, even with many loci, there can be substantial fluctuations in net adaptation, because at each locus, alleles randomly get lost or fixed. Thus, in a finite metapopulation, variation may gradually be lost by chance, even if it would persist in an infinite metapopulation. When conditions change across the whole metapopulation, there can be rapid change, which is predicted well by the fixed-state approximation. This work helps towards an understanding of how metapopulations extend their range across diverse environments. This article is part of the theme issue ‘Species’ ranges in the face of changing environments (Part II)’. AU - Barton, Nicholas H AU - Olusanya, Oluwafunmilola O ID - 10787 IS - 1848 JF - Philosophical Transactions of the Royal Society B: Biological Sciences KW - General Agricultural and Biological Sciences KW - General Biochemistry KW - Genetics and Molecular Biology SN - 0962-8436 TI - The response of a metapopulation to a changing environment VL - 377 ER - TY - JOUR AB - We analyse how migration from a large mainland influences genetic load and population numbers on an island, in a scenario where fitness-affecting variants are unconditionally deleterious, and where numbers decline with increasing load. Our analysis shows that migration can have qualitatively different effects, depending on the total mutation target and fitness effects of deleterious variants. In particular, we find that populations exhibit a genetic Allee effect across a wide range of parameter combinations, when variants are partially recessive, cycling between low-load (large-population) and high-load (sink) states. Increased migration reduces load in the sink state (by increasing heterozygosity) but further inflates load in the large-population state (by hindering purging). We identify various critical parameter thresholds at which one or other stable state collapses, and discuss how these thresholds are influenced by the genetic versus demographic effects of migration. Our analysis is based on a ‘semi-deterministic’ analysis, which accounts for genetic drift but neglects demographic stochasticity. We also compare against simulations which account for both demographic stochasticity and drift. Our results clarify the importance of gene flow as a key determinant of extinction risk in peripheral populations, even in the absence of ecological gradients. This article is part of the theme issue ‘Species’ ranges in the face of changing environments (part I)’. AU - Sachdeva, Himani AU - Olusanya, Oluwafunmilola O AU - Barton, Nicholas H ID - 10658 IS - 1846 JF - Philosophical Transactions of the Royal Society B SN - 0962-8436 TI - Genetic load and extinction in peripheral populations: The roles of migration, drift and demographic stochasticity VL - 377 ER - TY - JOUR AU - Barton, Nicholas H ID - 8112 IS - 1806 JF - Philosophical Transactions of the Royal Society. Series B: Biological Sciences SN - 0962-8436 TI - On the completion of speciation VL - 375 ER - TY - JOUR AB - Speciation, that is, the evolution of reproductive barriers eventually leading to complete isolation, is a crucial process generating biodiversity. Recent work has contributed much to our understanding of how reproductive barriers begin to evolve, and how they are maintained in the face of gene flow. However, little is known about the transition from partial to strong reproductive isolation (RI) and the completion of speciation. We argue that the evolution of strong RI is likely to involve different processes, or new interactions among processes, compared with the evolution of the first reproductive barriers. Transition to strong RI may be brought about by changing external conditions, for example, following secondary contact. However, the increasing levels of RI themselves create opportunities for new barriers to evolve and, and interaction or coupling among barriers. These changing processes may depend on genomic architecture and leave detectable signals in the genome. We outline outstanding questions and suggest more theoretical and empirical work, considering both patterns and processes associated with strong RI, is needed to understand how speciation is completed. AU - Kulmuni, Jonna AU - Butlin, Roger K. AU - Lucek, Kay AU - Savolainen, Vincent AU - Westram, Anja M ID - 8168 IS - 1806 JF - Philosophical Transactions of the Royal Society. Series B: Biological sciences SN - 0962-8436 TI - Towards the completion of speciation: The evolution of reproductive isolation beyond the first barriers VL - 375 ER - TY - JOUR AB - To prevent epidemics, insect societies have evolved collective disease defences that are highly effective at curing exposed individuals and limiting disease transmission to healthy group members. Grooming is an important sanitary behaviour—either performed towards oneself (self-grooming) or towards others (allogrooming)—to remove infectious agents from the body surface of exposed individuals, but at the risk of disease contraction by the groomer. We use garden ants (Lasius neglectus) and the fungal pathogen Metarhizium as a model system to study how pathogen presence affects self-grooming and allogrooming between exposed and healthy individuals. We develop an epidemiological SIS model to explore how experimentally observed grooming patterns affect disease spread within the colony, thereby providing a direct link between the expression and direction of sanitary behaviours, and their effects on colony-level epidemiology. We find that fungus-exposed ants increase self-grooming, while simultaneously decreasing allogrooming. This behavioural modulation seems universally adaptive and is predicted to contain disease spread in a great variety of host–pathogen systems. In contrast, allogrooming directed towards pathogen-exposed individuals might both increase and decrease disease risk. Our model reveals that the effect of allogrooming depends on the balance between pathogen infectiousness and efficiency of social host defences, which are likely to vary across host–pathogen systems. AU - Theis, Fabian AU - Ugelvig, Line V AU - Marr, Carsten AU - Cremer, Sylvia ID - 1830 IS - 1669 JF - Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences SN - 0962-8436 TI - Opposing effects of allogrooming on disease transmission in ant societies VL - 370 ER - TY - JOUR AB - Selection on one or more genes inevitably perturbs other genes, even when those genes have no direct effect on fitness. This article reviews the theory of such genetic hitchhiking, concentrating on effects on neutral loci. Maynard Smith and Haigh introduced the classical case where the perturbation is due to a single favourable mutation. This is contrasted with the apparently distinct effects of inherited variation in fitness due to loosely linked loci. A model of fluctuating selection is analysed which bridges these alternative treatments. When alleles sweep between extreme frequencies at a rate λ, the rate of drift is increased by a factor (1 + E[1/pq]λ/(2(2λ + r))), where the recombination rate r is much smaller than the strength of selection. In spatially structured populations, the effects of any one substitution are weaker, and only cause a local increase in the frequency of a neutral allele. This increase depends primarily on the rate of recombination relative to selection (r/s), and more weakly, on the neighbourhood size, Nb = 4πρσ2. Spatial subdivision may allow local selective sweeps to occur more frequently than is indicated by the overall rate of molecular evolution. However, it seems unlikely that such sweeps can be sufficiently frequent to increase significantly the drift of neutral alleles. AU - Barton, Nicholas H ID - 4274 IS - 1403 JF - Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences SN - 0962-8436 TI - Genetic hitchhiking VL - 355 ER - TY - JOUR AB - The evolutionary processes responsible for adaptation and speciation on islands differ in several ways from those on the mainland. Most attention has been given to the random genetic drift that arises when a population is founded from just a few colonizing genomes. Theoretical obstacles to 'founder effect speciation' are discussed, together with recent proposals for avoiding them. It is argued that although certain kinds of epistasis can facilitate the evolution of strong reproductive isolation, this favours divergence by selection as much as by random drift. AU - Barton, Nicholas H AU - Mallet, James ID - 3634 IS - 1341 JF - Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences SN - 0962-8436 TI - Natural selection and random genetic drift as causes of evolution on islands VL - 351 ER - TY - JOUR AB - Any sample of genes traces back to a single common ancestor. Each gene also has other properties: its sequence, its geographic location and the phenotype and fitness of the organism that carries it. With sexual reproduction, different genes have different genealogies, which gives us much more information, but also greatly complicates population genetic analysis. We review the close relation between the distribution of genealogies and the classic theory of identity by descent in spatially structured populations, and develop a simple diffusion approximation to the distribution of coalescence times in a homogeneous two-dimensional habitat. This shows that when neighbourhood size is large (as in most populations) only a small fraction of pairs of genes are closely related, and only this fraction gives information about current rates of gene flow. The increase of spatial dispersion with lineage age is thus a poor estimator of gene flow. The bulk of the genealogy depends on the long-term history of the population; we discuss ways of inferring this history from the concordance between genealogies across loci. AU - Barton, Nicholas H AU - Wilson, I ID - 3638 IS - 1327 JF - Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences SN - 0962-8436 TI - Genealogies and geography VL - 349 ER -