Inter-and intraspecific variation in fern mating systems after long-distance colonization: the importance of selfing

Diverse spore rains and limited local exchange shape fern genetic diversity in a recently created habitat colonized by long-distance dispersal

Although adaptationist hypotheses predict a functional relationship between mating systems and sexual size dimorphism, such predictions are difficult to test because of the high degree of phylogenetic conservatism in both of these traits. Taxa that show intraspecific variation in mating systems hence offer valuable opportunities for more direct tests of evolutionary-ecological hypotheses. Based on a collation of published and unpublished records, we document intraspecific geographic variation in mating systems (presence versus absence of male-male combat) within the widely-distributed Australian python Morelia spilota. Radiotelemetric monitoring of 19 free-ranging pythons in a population in north-eastern New South Wales showed that these animals display a mating system of female defence polygyny. Previous studies on a southern population of the same species found that males engaged in long mate-searching movements, showed no overt agonistic behavior, and formed long-term (>2 months) aggregations around reproductive females. In strong contrast, our adult male carpet pythons (i) moved about relatively little (mean displacement <11 m/day) during the mating season, (ii) remained with females only briefly (<5 days), and (iii) engaged in male-male combat in the vicinity of females. This male-male combat included vigorous biting as well as ritualised "wrestling" matches, resulting in a high incidence of bite scars in adult males. In keeping with predictions from sexual selection theory, males attain larger body sizes than females in this population, whereas females grow larger than males in the previously-studied southern population where males do not engage in physical combat for mating opportunities.

Seasonal variation in the mating system of a selfing annual with large floral displays.

Clarifying Baker's Law

Limited pollen flow and high selfing rates toward geographic range limit in an Atlantic forest bromeliad

Intraspecific variation in social systems is widely recognized across many taxa, and specific models, including polygamy potential, resource defense, and resource dispersion, have been developed to explain the relationship between ecological variation and social organization. Although mammals from temperate North America and Eurasia have provided many insights into this relationship, rodents from the Neotropics and temperate South America have largely been ignored. In this review we focus on reports documenting intraspecific variation in spacing systems, group size, and mating systems of caviomorphs. This large group of New World hystricognath rodents occupies a diverse array of habitats; thus, members of the same species potentially exhibit different social systems in response to different ecological conditions. Spatial patterns vary in response to a diverse array of factors, including predation, food availability, population density, and soil characteristics. Changes in group size typically correlate with changes in resource availability, particularly food. Mating systems generally reflect the ability of males to control access to females, which may depend on population density or food distribution. In general, social organization in caviomorphs fits predictions of resource-based models; however, most studies have been purely observational, involving small numbers of animals over short time periods and reporting qualitative rather than quantitative levels of ecological correlates. In future studies the use of molecular techniques and controlled, experimental manipulations can increase our understanding of intraspecific variation in caviomorph social systems. This understudied group of rodents offers excellent opportunities to provide insights into the influence of ecological conditions on behavior such as social systems.

The ability to self-fertilize is predicted to provide an advantage in colonization because a single individual can reproduce and establish a next generation in a new location regardless of the density of mates. While there is theoretical and correlative support for this idea, the strength of mate limitation as a selective agent has not yet been delineated from other factors that can also select for self-fertilization in colonization of new habitats. We used known mating-system variation in the American bellflower (Campanula americana) to explore how plants' ability to self-fertilize can mitigate density-dependent reproduction and impact colonization success. We created experimental populations of single individuals or a small number of plants to emulate isolated colonization events. These populations were composed of plants that differed in their ability to self-fertilize. We compared pollen limitation of the single individuals to that of small populations. Experimental populations of plants that readily self-fertilize produced consistent seed numbers regardless of population size, whereas plants with lower ability to self-fertilize had density-dependent reproduction with greater seed production in small populations than in populations composed of a single individual. We experimentally isolated the effect of mate limitation in colonization and found that it can select for increased self-fertilization. We show the benefit of self-fertilization in colonization, which helps to explain geographic patterns of self-fertilization and shows support for Baker's law, a long-held hypothesis in the field of mating-system evolution.

Phenology, the timing of recurrent life-history events, including bud bust, leaf out, flowering, fruiting, and leaf senescence, are related to environmental conditions and species interactions. As one of the most important plant functional traits, the qualitative correlation between inter- and intra-specific phenology variation and community structure has not been investigated at the community level. We monitored both flowering and fruiting phenology for 106 species during 2012 to 2015 in a Gutianshan 24ha permanent plot in a subtropical evergreen broad-leaved forest in Zhejiang province. We used standard deviation to evaluate inter-and intra-specific phenology variation. Results showed that precipitation was the major climatic factor influencing flowering phenology; most species flowered in May at the community level; fruiting phenology reached its peaks on October. Interspecific variation of flowering phenology was larger than that of fruiting phenology. The standard deviation of the interspecific variation of flowering phenology was 52, and of interspecific variation of fruiting phenology was 41. However, intraspecific variation on flowering phenology was smaller than fruiting. At the community level, intraspecific variation on flowering and fruiting phenology was smaller than intraspecific variations. Intraspecific variation on phenology at the community level was not significantly correlated with species abundance. Intraspecific variation of flowering phenology did not have a significant relationship with flowering date. However, intraspecific variation of fruiting phenology had a significant negative relationship with fruiting date. Intraspecific variation of fruiting phenology decreased as fruiting date increased. To our knowledge, this is the first study to explore the relationship between intraspecific phenology variation and phenology date and the first to evaluate the relationship between intraspecific phenology variation and species richness. Coupling these quantitative phenological data with community structure (abundance)will extend phenological analyses to understand how changes in phenology, andresulting changes in species interactions, affect fitness, an importantconcept for understanding the lasting impacts of phenological change, traits variation, and species diversification in the context of climate change.

Background and AimsUnderstanding patterns of pollen dispersal and variation in mating systems provides insights into the evolutionary potential of plant species and how historically rare species with small disjunct populations persist over long time frames. This study aims to quantify the role of pollen dispersal and the mating system in maintaining contemporary levels of connectivity and facilitating persistence of small populations of the historically rare Acacia woodmaniorum.MethodsProgeny arrays of A. woodmaniorum were genotyped with nine polymorphic microsatellite markers. A low number of fathers contributed to seed within single pods; therefore, sampling to remove bias of correlated paternity was implemented for further analysis. Pollen immigration and mating system parameters were then assessed in eight populations of varying size and degree of isolation.Key ResultsPollen immigration into small disjunct populations was extensive (mean minimum estimate 40 % and mean maximum estimate 57 % of progeny) and dispersal occurred over large distances (≤1870m). Pollen immigration resulted in large effective population sizes and was sufficient to ensure adaptive and inbreeding connectivity in small disjunct populations. High outcrossing (mean tm = 0·975) and a lack of apparent inbreeding suggested that a self-incompatibility mechanism is operating. Population parameters, including size and degree of geographic disjunction, were not useful predictors of pollen dispersal or components of the mating system.ConclusionsExtensive long-distance pollen dispersal and a highly outcrossed mating system are likely to play a key role in maintaining genetic diversity and limiting negative genetic effects of inbreeding and drift in small disjunct populations of A. woodmaniorum. It is proposed that maintenance of genetic connectivity through habitat and pollinator conservation will be a key factor in the persistence of this and other historically rare species with similar extensive long-distance pollen dispersal and highly outcrossed mating systems.

Western redcedar (Thuja plicata, Cupressaceae) is a self-fertile conifer with a mixed mating system and significant variation for outcrossing among populations. In this paper, we conducted a fine-scale study of mating system variation to identify correlates of outcrossing in natural populations. We examined variation for outcrossing within and among individual trees, and describe a new method to estimate outcrossing using bulked DNA samples. Bulking (assaying DNA tissues from several individuals simultaneously) increases the experimental power without increasing the experimental effort. We sampled 80 trees from four natural populations in southwestern British Columbia. From each tree, we sampled from up to six crown positions (three heights and inner vs outer branches). From each position, two samples of three seedlings each were bulked before DNA extractions. Using four microsatellite loci, we obtained outcrossing rates for each tree and for each of the six crown positions. We found individual tree selfing rates to increase with tree height in all four populations, but selfing rates did not differ among crown positions. The higher selfing rate of larger trees is probably due to their greater proportional contribution to local pollen clouds. Individual tree outcrossing rates ranged from 22 to 100% and the population outcrossing rates from 66 to 78%. Missed alleles due to bulking and the estimation method used both cause a downward bias in outcrossing rates, so that these estimates are probably lower than the actual outcrossing rates. Nevertheless, the trends we observed are not affected by systematic biases of estimation.

The frequency of outcrossing in two hybridizing species of Iris was estimated for populations and for individual fruits. Effects of floral phenology and the local densities of flowers on outcrossing rates were examined and the potential for hybrid seed formation under different pollen environments was assessed. The populations examined differed with respect to the spatial distribution of plants and the level of genetic structure; the I. fulva population consisted of a number of low density patches and appeared to have some genetic differentiation whereas the I. hexagona population consisted of a single high-density experimental plot of randomly distributed genotypes. Population outcrossing rate estimates were relatively high (0.67–0.90) for both species. The distribution of family outcrossing rates tended to be bimodal for both species with individual fruits either having the majority of seeds fertilized by outcrossed donors or being almost entirely selfed. The frequency of outcrossed fruits increased with the number of flowers open at other plants and decreased when more flowers were open on the same stem in I. hexagona. In I. fulva the opposite trends were apparent; outcrossing decreased when more flowers were open on other stems and increased when more flowers were open on the same stem. The unexpected responses of outcrossing frequency in I. fulva may have been a consequence of higher levels of vegetative reproduction and genetic structure and the behaviour of pollen vectors. Differences in pollen prepotency and the higher selfing rates observed at low floral densities in I. hexagona may have contributed to the observed patterns of hybrid seed formation. The analyses of family outcrossing rates provide important information on factors responsible for mating system variation and evolution.

Crow et al. (1990) and Barton (1992) have examined the critical migration rate for swamping selection in the nuclear system. Here, I use the same methodology to examine the critical migration rate in the cytonuclear system for hermaphrodite plants with a mixed mating system. Two selection schemes for a nuclear gene (heterozygote disadvantage and directional selection) and the directional selection scheme for organelle genes are considered. Results show that under random mating, the previous results are applicable to plant species by appropriate re-parameterization of the migration rate for nuclear and paternal organelle genes. A simple complementary relationship exists between seed and pollen flow in contributing to the critical migration rate. Under the mixed mating system, the critical migration rate of seeds and pollen for nuclear and paternal organelle genes can be changed due to the effects of selection and the cytonuclear linkage disequilibrium generated by migration and inbreeding. A negative but not complementary relationship exists between seed and pollen flow in contributing to the critical migration rate, varying with the mating system. Partial selfing can also adjust the critical seed flow for the maternal organelle gene, with a small critical migration rate for species of a high selfing rate. Both concordance and discordance among cytonuclear genes can occur under certain conditions during the process of swamping selection. This theory predicts the presence of various contributions of seed versus pollen flow to genetic swamping for plants with diverse mating systems.

Fewer than 1% of vertebrate species are hermaphroditic, and essentially all of these are fishes. Four types of hermaphroditism are known in fishes: simultaneous (or synchronous) hermaphroditism (SH), protandry (male-to-female sex change; PA), protogyny (female-to-male sex change; PG), and bidirectional sex change (BS or reversed sex change in protogynous species). Here we present an annotated list of hermaphroditic fish species from a comprehensive review and careful re-examination of all primary literature. We confirmed functional hermaphroditism in more than 450 species in 41 families of 17 teleost orders. PG is the most abundant type (305 species of 20 families), and the others are much less abundant, BS in 66 species of seven families, SH in 55 species of 13 families, and PA in 54 species of 14 families. The recently proposed phylogenetic tree indicated that SH and PA have evolved several times in not-closely related lineages of Teleostei but that PG (and BS) has evolved only in four lineages of Percomorpha. Examination of the relation between hermaphroditism type and mating system in each species mostly supported the size-advantage model that predicts the evolution of sequential hermaphroditism. Finally, intraspecific variations in sexual pattern are discussed in relation to population density, which may cause variation in mating system.

Linking species and ecosystems often relies on approaches that consider how the traits exhibited by species affect ecosystem processes. One method is to estimate functional diversity (FD) based on the dispersion of species in functional trait space. Individuals within a species also differ, however, and an unresolved challenge is how to include such intraspecific variability in a measure of functional diversity. Our solution is to extend an existing measure to variation among individuals within species. Here, simulations demonstrate how the new measure behaves relative to one that does not include individual variation. Individual-level FD was less well associated with species richness than species-level FD in a single trait dimension, because species differed in their intraspecific variation. However, in multiple trait dimensions, there was a strong association between individual- and species-level FD and richness, because many traits result in a tight relationship between functional diversity and species richness. The correlation between the two FD measures weakened as the amount of intraspecific variability increased. Analyzing natural plant communities we found no relationship between species richness and functional diversity. In these analyses, we did not have to specify the source of intraspecific variation. In fact, the variation was only among individuals. The measure can, however, include differences in the amount of intraspecific variation at different sites, as we demonstrate. Including intraspecific variation should allow a more complete understanding of the processes that link individuals and ecosystems and provide better predictions about the consequences of extinctions for ecosystem processes.

Baker's law refers to the tendency for species that establish on islands by long-distance dispersal to show an increased capacity for self-fertilization because of the advantage of self-compatibility when colonizing new habitat. Despite its intuitive appeal and broad empirical support, it has received substantial criticism over the years since it was proclaimed in the 1950s, not least because it seemed to be contradicted by the high frequency of dioecy on islands. Recent theoretical work has again questioned the generality and scope of Baker's law. Here, we attempt to discern where the idea is useful to apply and where it is not. We conclude that several of the perceived problems with Baker's law fall away when a narrower perspective is adopted on how it should be circumscribed. We emphasize that Baker's law should be read in terms of an enrichment of a capacity for uniparental reproduction in colonizing situations, rather than of high selfing rates. We suggest that Baker's law might be tested in four different contexts, which set the breadth of its scope: the colonization of oceanic islands, metapopulation dynamics with recurrent colonization, range expansions with recurrent colonization, and colonization through species invasions.