Seascape drivers of Macrocystis pyrifera population genetic structure in the northeast Pacific

At small spatial and temporal scales, genetic differentiation is largely controlled by constraints on gene flow, while genetic diversity across a species' distribution is shaped on longer temporal and spatial scales. We assess the hypothesis that oceanographic transport and other seascape features explain different scales of genetic structure of giant kelp, Macrocystis pyrifera. We followed a hierarchical approach to perform a microsatellite‐based analysis of genetic differentiation in Macrocystis across its distribution in the northeast Pacific. We used seascape genetic approaches to identify large‐scale biogeographic population clusters and investigate whether they could be explained by oceanographic transport and other environmental drivers. We then modelled population genetic differentiation within clusters as a function of oceanographic transport and other environmental factors. Five geographic clusters were identified: Alaska/Canada, central California, continental Santa Barbara, California Channel Islands and mainland southern California/Baja California peninsula. The strongest break occurred between central and southern California, with mainland Santa Barbara sites forming a transition zone between the two. Breaks between clusters corresponded approximately to previously identified biogeographic breaks, but were not solely explained by oceanographic transport. An isolation‐by‐environment (IBE) pattern was observed where the northern and southern Channel Islands clustered together, but not with closer mainland sites, despite the greater distance between them. The strongest environmental association with this IBE pattern was observed with light extinction coefficient, which extends suitable habitat to deeper areas. Within clusters, we found support for previous results showing that oceanographic connectivity plays an important role in the population genetic structure of Macrocystis in the Northern hemisphere.     

Joint evolution of differential seed dispersal and self‐fertilization

Differential seed dispersal, in which selfed and outcrossed seeds possess different dispersal propensities, represents a potentially important individual‐level association. A variety of traits can mediate differential seed dispersal, including inflorescence and seed size variation. However, how natural selection shapes such associations is poorly known. Here, we developed theoretical models for the evolution of mating system and differential seed dispersal in metapopulations, incorporating heterogeneous pollination, dispersal cost, cost of outcrossing and environment‐dependent inbreeding depression. We considered three models. In the ‘fixed dispersal model’, only selfing rate is allowed to evolve. In the ‘fixed selfing model’, in which selfing is fixed but differential seed dispersal can evolve, we showed that natural selection favours a higher, equal or lower dispersal rate for selfed seeds to that for outcrossed seeds. However, in the ‘joint evolution model’, in which selfing and dispersal can evolve together, evolution necessarily leads to higher or equal dispersal rate for selfed seeds compared to that for outcrossed. Further comparison revealed that outcrossed seed dispersal is selected against by the evolution of mixed mating or selfing, whereas the evolution of selfed seed dispersal undergoes independent processes. We discuss the adaptive significance and constraints for mating system/dispersal association.     

Experimental and genetic analyses reveal that inbreeding depression declines with increased self‐fertilization among populations of a coastal dune plant

Theory predicts that inbreeding depression (ID) should decline via purging in self‐fertilizing populations. Yet, intraspecific comparisons between selfing and outcrossing populations are few and provide only mixed support for this key evolutionary process. We estimated ID for large‐flowered (LF), predominantly outcrossing vs. small‐flowered (SF), predominantly selfing populations of the dune endemic Camissoniopsis cheiranthifolia by comparing selfed and crossed progeny in glasshouse environments differing in soil moisture, and by comparing allozyme‐based estimates of the proportion of seeds selfed and inbreeding coefficient of mature plants. Based on lifetime measures of dry mass and flower production, ID was stronger in nine LF populations [mean δ = 1?(fitness of selfed seed/fitness of outcrossed seed) = 0.39] than 16 SF populations (mean δ = 0.03). However, predispersal ID during seed maturation was not stronger for LF populations, and ID was not more pronounced under simulated drought, a pervasive stress in sand dune habitat. Genetic estimates of δ were also higher for four LF (δ = 1.23) than five SF (δ = 0.66) populations; however, broad confidence intervals around these estimates overlapped. These results are consistent with purging, but selective interference among loci may be required to maintain strong ID in partially selfing LF populations, and trade‐offs between selfed and outcrossed fitness are likely required to maintain outcrossing in SF populations.     

Isolation by oceanographic distance explains genetic structure for Macrocystis pyrifera in the Santa Barbara Channel

Ocean currents are expected to be the predominant environmental factor influencing the dispersal of planktonic larvae or spores; yet, their characterization as predictors of marine connectivity has been hindered by a lack of understanding of how best to use oceanographic data. We used a high-resolution oceanographic model output and Lagrangian particle simulations to derive oceanographic distances (hereafter called transport times) between sites studied for Macrocystis pyrifera genetic differentiation. We build upon the classical isolation-by-distance regression model by asking how much additional variability in genetic differentiation is explained when adding transport time as predictor. We explored the extent to which gene flow is dependent upon seasonal changes in ocean circulation. Because oceanographic transport between two sites is inherently asymmetric, we also compare the explanatory power of models using the minimum or the mean transport times. Finally, we compare the direction of connectivity as estimated by the oceanographic model and genetic assignment tests. We show that the minimum transport time had higher explanatory power than the mean transport time, revealing the importance of considering asymmetry in ocean currents when modelling gene flow. Genetic assignment tests were much less effective in determining asymmetry in gene flow. Summer-derived transport times, in particular for the month of June, which had the strongest current speed, greatest asymmetry and highest spore production, resulted in the best-fit model explaining twice the variability in genetic differentiation relative to models that use geographic distance or habitat continuity. The best overall model also included habitat continuity and explained 65% of the variation in genetic differentiation among sites.     

The joint evolution of lifespan and self‐fertilization

In Angiosperms, there exists a strong association between mating system and lifespan. Most self‐fertilizing species are short‐lived, and most predominant or obligate outcrossers are long‐lived. This association is generally explained by the influence of lifespan on the evolution of the mating system, considering lifespan as fixed. Yet, lifespan can itself evolve, and the mating system may as well influence the evolution of lifespan, as is suggested by joint evolutionary shifts of lifespan and mating system between sister species. In this paper, we build modifier models to study the joint evolution of self‐fertilization and lifespan, including both juvenile and adult inbreeding depression. We show that provided that inbreeding depression affects adult survival, self‐fertilization is expected to promote evolution towards shorter lifespan, and that the range of conditions under which selfing can evolve rapidly shrinks as lifespan increases. We study the effects of inbreeding depression affecting various steps in the life cycle and discuss how extrinsic mortality conditions are expected to affect evolutionary associations. In particular, we show that selfers may sometimes remain short‐lived even in a very stable habitat, as a strategy to avoid the deleterious effects of inbreeding.     

The influence of self‐fertilization and grouping on fitness attributes in the freshwater snail Physa acuta: population and individual inbreeding depression

The genetic structure, selfing rate and inbreeding depression of the hermaphroditic freshwater snail Physa acuta were jointly analysed in a population near Montpellier, France. Allozymic markers revealed moderate gene diversity (0.138), and no heterozygote deficiency. The mean outcrossing rate, estimated by using progeny arrays, was 0.9, with substantial variation among families. This also suggests that the number of fathers among outcrossed offspring of a given mother is low. Inbreeding depression was estimated over more than one generation using 83 first‐laboratory‐generation (G₁) families. The main parameters measured were parental (G₁) fecundity, offspring (G₂) survival and fecundity. Size and growth were also monitored. Parental fecundity was analysed under several conditions (isolation, pair and quadruplet outcrossing). The self‐fertilization depression, including parental fecundity, offspring survival and fecundity, was about 0.9 at the population level. The genetic data obtained in the same population indicate a value of about 0.3 using Ritland’s (1990) technique, suggesting that the depression over the whole life‐cyle might be even higher than 0.9. Grouping affected neither fecundity nor self‐fertilization depression. Substantial variation in depression for survival was detected among individuals, from no survival in some selfed families to better survival than that of outbred families in others. The overall result (outbred population structure, high outcrossing rate and high self‐fertilization depression) is consistent with what is expected in large outcrossing populations in which inbreeding depression is maintained by mutation‐selection balance.     

Evolution towards self‐compatibility when mates are limited

Theory of plant mating system evolution predicts the spread of self‐compatibility (SC) in a predominantly self‐incompatible population when inbreeding depression (ID; the decline in fitness because of selfing) is small and when compatible mates are limited. I tested these two predictions by measuring the occurrence of SC in 13 natural populations of Ranunculus reptans L. that varied in ID and frequency of cross‐incompatible mates. Enforced selfing experiments were conducted in 2 years. In the first year, self‐pollination was applied at two flower ages to investigate the occurrence of delayed SC. I found that SC was not uncommon across all populations, but self‐compatible plants usually produced few seeds. There was no evidence for delayed SC. The occurrence of SC was not associated with population‐level ID, but populations with more limited availability of compatible mates had a significantly higher frequency of plants that were at least partially self‐compatible. The results indicate that, in R. reptans, a shortage of available mates in small populations may cause the evolution of partial SC and mixed mating.     

Costs of selfing prevent the spread of a self‐compatibility mutation that causes reproductive assurance

In flowering plants, shifts from outcrossing to partial or complete self‐fertilization have occurred independently thousands of times, yet the underlying adaptive processes are difficult to discern. Selfing's ability to provide reproductive assurance when pollination is uncertain is an oft‐cited ecological explanation for its evolution, but this benefit may be outweighed by costs diminishing its selective advantage over outcrossing. We directly studied the fitness effects of a self‐compatibility mutation that was backcrossed into a self‐incompatible (SI) population of Leavenworthia alabamica, illuminating the direction and magnitude of selection on the mating‐system modifier. In array experiments conducted in two years, self‐compatible (SC) plants produced 17–26% more seed, but this advantage was counteracted by extensive seed discounting—the replacement of high‐quality outcrossed seeds by selfed seeds. Using a simple model and simulations, we demonstrate that SC mutations with these attributes rarely spread to high frequency in natural populations, unless inbreeding depression falls below a threshold value (0.57 ≤ δ_threshold ≤ 0.70) in SI populations. A combination of heavy seed discounting and inbreeding depression likely explains why outcrossing adaptations such as self‐incompatibility are maintained generally, despite persistent input of selfing mutations, and frequent limits on outcross seed production in nature.     

Turnover in local parasite populations temporarily favors host outcrossing over self‐fertilization during experimental evolution

The ubiquity of outcrossing in plants and animals is difficult to explain given its costs relative to self‐fertilization. Despite these costs, exposure to changing environmental conditions can temporarily favor outcrossing over selfing. Therefore, recurring episodes of environmental change are predicted to favor the maintenance of outcrossing. Studies of host–parasite coevolution have provided strong support for this hypothesis. However, it is unclear whether multiple exposures to novel parasite genotypes in the absence of coevolution are sufficient to favor outcrossing. Using the nematode Caenorhabditis elegans and the bacterial parasite Serratia marcescens, we studied host responses to parasite turnover. We passaged several replicates of a host population that was well‐adapted to the S. marcescens strain Sm2170 with either Sm2170 or one of three novel S. marcescens strains, each derived from Sm2170, for 18 generations. We found that hosts exposed to novel parasites maintained higher outcrossing rates than hosts exposed to Sm2170. Nonetheless, host outcrossing rates declined over time against all but the most virulent novel parasite strain. Hosts exposed to the most virulent novel strain exhibited increased outcrossing rates for approximately 12 generations, but did not maintain elevated levels of outcrossing throughout the experiment. Thus, parasite turnover can transiently increase host outcrossing. These results suggest that recurring episodes of parasite turnover have the potential to favor the maintenance of host outcrossing. However, such maintenance may require frequent exposure to novel virulent parasites, rapid rates of parasite turnover, and substantial host gene flow.     

A field test of a model for the stability of androdioecy in the freshwater shrimp,Eulimnadia texana

The evolution of hermaphroditism from dioecy is a poorly studied transition. Androdioecy (the coexistence of males and hermaphrodites) has been suggested as an intermediate step in this evolutionary transition or could be a stable reproductive mode. Freshwater crustaceans in the genus Eulimnadia have reproduced via androdioecy for 24+ million years and thus are excellent organisms to test models of the stability of androdioecy. Two related models that allow for the stable maintenance of males and hermaphrodites rely on the counterbalancing of three life history parameters. We tested these models in the field over three field seasons and compared the results to previous laboratory estimates of these three parameters. Male and hermaphroditic ratios within years were not well predicted using either the simpler original model or a version of this model updated to account for differences between hermaphroditic types (‘monogenic’ and ‘amphigenic’ hermaphrodites). Using parameter estimates of the previous year to predict the next year's sex ratios revealed a much better fit to the original relative to the updated version of the model. Therefore, counter to expectations, accounting for differences between the two hermaphroditic types did not improve the fit of these models. At the moment, we lack strong evidence that the long‐term maintenance of androdioecy in these crustaceans is the result of a balancing of life history parameters; other factors, such as metapopulation dynamics or evolutionary constraints, may better explain the 24+ million year maintenance of androdioecy in clam shrimp.     

The genetic architecture of tristyly and its breakdown to self‐fertilization

The floral polymorphism tristyly involves three style morphs with a reciprocal arrangement of stigma and anther heights governed by two diallelic loci (S and M). Tristyly functions to promote cross‐pollination, but modifications to stamen position commonly cause transitions to selfing. Here, we integrate whole‐genome sequencing and genetic mapping to investigate the genetic architecture of the M locus and the genetic basis of independent transitions to selfing in tristylous Eichhornia paniculata. We crossed independently derived semi‐homostylous selfing variants of the long‐ and mid‐styled morph fixed for alternate alleles at the M locus (ssmm and ssMM, respectively), and backcrossed the F₁ to the parental ssmm genotype. We phenotyped and genotyped 462 backcross progeny using 1450 genotyping‐by‐sequencing (GBS) markers and performed composite interval mapping to identify quantitative trait loci (QTL) governing style‐length and anther‐height variation. A QTL associated with the primary style‐morph differences (style length and anther height) mapped to linkage group 5 and spanned ~13–27.5 Mbp of assembled sequence. Bulk segregant analysis identified 334 genes containing SNPs potentially linked to the M locus. The stamen modifications characterizing each selfing variant were governed by loci on different linkage groups. Our results provide an important step towards identifying the M locus and demonstrate that transitions to selfing have originated by independent sets of mating‐system modifier genes unlinked to the M locus, a pattern inconsistent with a recombinational origin of selfing variants at a putative supergene.     

Extrapair fertilization and genetic similarity of social mates in the Mexican jay

Inbreeding depression should favor the ability of females toavoid inbreeding or minimize its effects. We tested for a relationshipbetween genetic similarity of social pairs and the occurrenceof extrapair fertilization (EPF) in the Mexican jay (Aphelocomaultramarina). Multilocus minisatellite and microsatellite DNAfingerprinting was used to detect extrapair young and measuregenetic similarity between social parents. We found that 12of 31 (39%) nests had at least one EPF and 15 of 93 (16%) youngwere the result of EPF. The mean DNA fingerprinting band sharingscore between social mates who had at least one EPF was significantlyhigher than the mean band sharing score between mates who didnot (0.35 versus 0.25). The mean band sharing score for non-EPFdyads (0.25) was similar to the background band sharing amongnonrelatives (0.23). The mean band sharing score for mates thathad an EPF was significantly higher than that of nonrelatives(background) and was significantly lower than that of half-siblings(0.52). Our results showed a highly significant relationshipbetween genetic similarity of social mates and incidence ofEPF.     

The decline in fitness with inbreeding: evidence for negative dominance‐by‐dominance epistasis in Drosophila melanogaster

Genetic interactions can play an important role in the evolution of reproductive strategies. In particular, negative dominance‐by‐dominance epistasis for fitness can theoretically favour sex and recombination. This form of epistasis can be detected statistically because it generates nonlinearity in the relationship between fitness and inbreeding coefficient. Measures of fitness in progressively inbred lines tend to show limited evidence for epistasis. However, tests of this kind can be biased against detecting an accelerating decline due to line losses at higher inbreeding levels. We tested for dominance‐by‐dominance epistasis in Drosophila melanogaster by examining viability at five inbreeding levels that were generated simultaneously, avoiding the bias against detecting nonlinearity that has affected previous studies. We find an accelerating rate of fitness decline with inbreeding, indicating that dominance‐by‐dominance epistasis is negative on average, which should favour sex and recombination.     

TRANSMISSION ADVANTAGE FAVORS SELFING ALLELE IN EXPERIMENTAL POPULATIONS OF SELF‐INCOMPATIBLE WITHERINGIA SOLANACEA (SOLANACEAE)

The evolution of self‐fertilization is one of the most commonly traversed transitions in flowering plants, with profound implications for population genetic structure and evolutionary potential. We investigated factors influencing this transition using Witheringia solanacea, a predominantly self‐incompatible (SI) species within which self‐compatible (SC) genotypes have been identified. We showed that self‐compatibility in this species segregates with variation at the S‐locus as inherited by plants in F1 and F2 generations. To examine reproductive assurance and the transmission advantage of selfing, we placed SC and SI genotypes in genetically replicated gardens and monitored male and female reproductive success, as well as selfing rates of SC plants. Self‐compatibility did not lead to increased fruit or seed set, even under conditions of pollinator scarcity, and the realized selfing rate of SC plants was less than 10%. SC plants had higher fruit abortion rates, consistent with previous evidence showing strong inbreeding depression at the embryonic stage. Although the selfing allele did not provide reproductive assurance under observed conditions, it also did not cause pollen discounting, so the transmission advantage of selfing should promote its spread. Given observed numbers of S‐alleles and selfing rates, self‐compatibility should spread even under conditions of exceedingly high initial inbreeding depression.     

Genetic rescue by distant trees mitigates qualitative pollen limitation imposed by fine‐scale spatial genetic structure

Restricted seed dispersal frequently leads to fine‐scale spatial genetic structure (i.e., FSGS) within plant populations. Depending on its spatial extent and the mobility of pollinators, this inflated kinship at the immediate neighbourhood can critically impoverish pollen quality. Despite the common occurrence of positive FSGS within plant populations, our knowledge regarding the role of long‐distance pollination preventing reproductive failure is still limited. Using microsatellite markers, we examined the existence of positive FSGS in two low‐density populations of the tree Pyrus bourgaeana. We also designed controlled crosses among trees differing in their kinship to investigate the effects of increased local kinship on plant reproduction. We used six pollination treatments and fully monitored fruit production, fruit and seed weight, proportion of mature seeds per fruit, and seed germination. Our results revealed positive FSGS in both study populations and lower fruit initiation in flowers pollinated with pollen from highly‐genetically related individuals within the neighbourhood, with this trend intensifying as the fruit development progressed. Besides, open‐pollinated flowers exhibited lower performance compared to those pollinated by distant pollen donors, suggesting intense qualitative pollen limitation in natural populations. We found positive fine‐scale spatial genetic structure is translated into impoverished pollen quality from nearby pollen donors which negatively impacts the reproductive success of trees in low‐density populations. Under this scenario of intrapopulation genetic rescue by distant pollen donors, the relevance of highly‐mobile pollinators for connecting spatially and genetically distant patches of trees may be crucial to safeguarding population recruitment.     

Repeated evolution and reversibility of self‐fertilization in the volvocine green algae*

Outcrossing and self‐fertilization are fundamental strategies of sexual reproduction, each with different evolutionary costs and benefits. Self‐fertilization is thought to be an evolutionary “dead‐end” strategy, beneficial in the short term but costly in the long term, resulting in self‐fertilizing species that occupy only the tips of phylogenetic trees. Here, we use volvocine green algae to investigate the evolution of self‐fertilization. We use ancestral‐state reconstructions to show that self‐fertilization has repeatedly evolved from outcrossing ancestors and that multiple reversals from selfing to outcrossing have occurred. We use three phylogenetic metrics to show that self‐fertilization is not restricted to the tips of the phylogenetic tree, a finding inconsistent with the view of self‐fertilization as a dead‐end strategy. We also find no evidence for higher extinction rates or lower speciation rates in selfing lineages. We find that self‐fertilizing species have significantly larger colonies than outcrossing species, suggesting the benefits of selfing may counteract the costs of increased size. We speculate that our macroevolutionary results on self‐fertilization (i.e., non‐tippy distribution, no decreased diversification rates) may be explained by the haploid‐dominant life cycle that occurs in volvocine algae, which may alter the costs and benefits of selfing.     

Mixed pollen load and late‐acting self‐incompatibility flexibility in Adenocalymma peregrinum (Miers) L.G. Lohmann (Bignonieae: Bignoniaceae)

• Mixed cross and self‐pollen load on the stigma (mixed pollination) of species with late‐acting self‐incompatibility system (LSI) can lead to self‐fertilized seed production. This “cryptic self‐fertility” may allow selfed seedling development in species otherwise largely self‐sterile. Our aims were to check if mixed pollinations would lead to fruit set in LSI Adenocalymma peregrinum, and test for evidence of early‐acting inbreeding depression in putative selfed seeds from mixed pollinations.
• Experimental pollinations were carried out in a natural population. Fruit and seed set from self‐, cross and mixed pollinations were analysed. Further germination tests were carried out for the seeds obtained from treatments.
• Our results confirm self‐incompatibility, and fruit set from cross‐pollinations was three‐fold that from mixed pollinations. This low fruit set in mixed pollinations is most likely due to a greater number of self‐ than cross‐fertilized ovules, which promotes LSI action and pistil abortion. Likewise, higher percentage of empty seeds in surviving fruits from mixed pollinations compared with cross‐pollinations is probably due to ovule discounting caused by self‐fertilization. Moreover, germinability of seeds with developed embryos was lower in fruits from mixed than from cross‐pollinations, and the non‐viable seeds from mixed pollinations showed one‐third of the mass of those from cross‐pollinations.
• The great number of empty seeds, lower germinability, lower mass of non‐viable seeds, and higher variation in seed mass distribution in mixed pollinations, strongly suggests early‐acing inbreeding depression in putative selfed seeds. In this sense, LSI and inbreeding depression acting together probably constrain self‐fertilized seedling establishment in A. peregrinum.

     

The double edged sword: The demographic consequences of the evolution of self‐fertilization

Phylogenies indicate that the transition from outcrossing to selfing is frequent, with selfing populations being more prone to extinction. The rates of transition to selfing and extinction, acting on different timescales, could explain the observed distributions of extant selfing species among taxa. However, phylogenetic and theoretical studies consider these mechanisms independently, that is transitions do not cause extinction. Here, we theoretically explore the demographic consequences of the evolution of self‐fertilization. Deleterious mutations and mutations modifying the selfing rate are recurrently introduced and the number of offspring depends on individual fitness, allowing for a demographic feedback. We show that mutational meltdowns can be triggered in populations evolving near strict selfing. Populations having survived a demographic crash are more stable than ancestral outcrossing populations once deleterious mutations are purged. The relatively rapid time‐scales at which extinctions occur indicate that during evolutionary transitions the accumulation of deleterious mutations may not be the cause of extinctions observed on longer time scales, but could lead to the underestimation of transition rates from outcrossing to selfing.     

Microsatellite diversity and genetic structure of fragmented populations of the rare,fire-dependent shrub Grevillea macleayana

Recent habitat loss and fragmentation superimposed upon ancient patterns of population subdivision are likely to have produced low levels of neutral genetic diversity and marked genetic structure in many plant species. The genetic effects of habitat fragmentation may be most pronounced in species that form small populations, are fully self-compatible and have limited seed dispersal. However, long-lived seed banks, mobile pollinators and long adult lifespans may prevent or delay the accumulation of genetic effects. We studied a rare Australian shrub species, Grevillea macleayana (Proteaceae), that occurs in many small populations, is self-compatible and has restricted seed dispersal. However, it has a relatively long adult lifespan (c. 30 years), a long-lived seed bank that germinates after fire and is pollinated by birds that are numerous and highly mobile. These latter characteristics raise the possibility that populations in the past may have been effectively large and genetically homogeneous. Using six microsatellites, we found that G. macleayana may have relatively low within-population diversity (3.2-4.2 alleles/locus; Hexp = 0.420-0.530), significant population differentiation and moderate genetic structure (FST = 0.218) showing isolation by distance, consistent with historically low gene flow. The frequency distribution of allele sizes suggest that this geographical differentiation is being driven by mutation. We found a lack mutation-drift equilibrium in some populations that is indicative of population bottlenecks. Combined with evidence for large spatiotemporal variation of selfing rates, this suggests that fluctuating population sizes characterize the demography in this species, promoting genetic drift. We argue that natural patterns of pollen and seed dispersal, coupled with the patchy, fire-shaped distribution, may have restricted long-distance gene flow in the past.     

Heterogeneity in local density allows a positive evolutionary relationship between self‐fertilisation and dispersal

Despite empirical evidence for a positive relationship between dispersal and self‐fertilization (selfing), theoretical work predicts that these traits should always be negatively correlated, and the Good Coloniser Syndrome of high dispersal and selfing (Cf. Baker's Law) should not evolve. Critically, previous work assumes that adult density is spatiotemporally homogeneous, so selfing results in identical offspring production for all patches, eliminating the benefit of dispersal for escaping from local resource competition. We investigate the joint evolution of dispersal and selfing in a demographically structured metapopulation model where local density is spatiotemporally heterogeneous due to extinction‐recolonization dynamics. Selfing alleviates outcrossing failure due to low local density (an Allee effect) while dispersal alleviates competition through dispersal of propagules from high‐ to low‐density patches. Because local density is spatiotemporally heterogeneous in our model, selfing does not eliminate heterogeneity in competition, so dispersal remains beneficial even under full selfing. Hence the Good Coloniser Syndrome is evolutionarily stable under a broad range of conditions, and both negative and positive relationships between dispersal and selfing are possible, depending on the environment. Our model thus accommodates positive empirical relationships between dispersal and selfing not predicted by previous theoretical work and provides additional explanations for negative relationships.