Do specialized flowers promote reproductive isolation? Realized pollination accuracy of three sympatric Pedicularis species

Background and Aims

Interest in pollinator-mediated evolutionary divergence of flower phenotype and speciation in plants has been at the core of plant evolutionary studies since Darwin. Specialized pollination is predicted to lead to reproductive isolation and promote speciation among sympatric species by promoting partitioning of (1) the species of pollinators used, (2) when pollinators are used, or (3) the sites of pollen placement. Here this last mechanism is investigated by observing the pollination accuracy of sympatric Pedicularis species (Orobanchacae).

Methods

Pollinator behaviour was observed on three species of Pedicularis (P. densispica, P. tricolor and P. dichotoma) in the Hengduan Mountains, south-west China. Using fluorescent powder and dyed pollen, the accuracy was assessed of stigma contact with, and pollen deposition on, pollinating bumble-bees, respectively.

Key Results

All three species of Pedicularis were pollinated by bumble-bees. It was found that the adaptive accuracy of female function was much higher than that of male function in all three flower species. Although peak pollen deposition corresponded to the optimal location on the pollinator (i.e. the site of stigma contact) for each species, substantial amounts of pollen were scattered over much of the bees'' bodies.

Conclusions

The Pedicularis species studied in the eastern Himalayan region did not conform with Grant''s ‘Pedicularis Model’ of mechanical reproductive isolation. The specialized flowers of this diverse group of plants seem unlikely to have increased the potential for reproductive isolation or influenced rates of speciation. It is suggested instead that the extreme species richness of the Pedicularis clade was generated in other ways and that specialized flowers and substantial pollination accuracy evolved as a response to selection generated by the diversity of co-occurring congeners.     

The relative of species pools in determining plant species richness: an alternative explanation of species coexistence?

Explanations of the pattern of species have traditionally relied on small-scale, local processes occurring in ecological time. Differences in species richness have associated with different mechanisms avoiding competition, such as spatiotemporal heterogeneity (weaker competitors may find a more favourable place or time) or environmental stress (competition is assumed to be less intensive under difficult conditions). More recently, large-scale process have been taken into account, raising such questions as: which plant species may potentially grow in a certain community? Are evolutionary processes and species dispersal responsible for the differences between communities? The species-pool theory attempts to answer these general questions, and information about species pools is needed for the design of experiments where the number of species in a community is manipulated.     

A new hypothesis for species coexistence: male–male repulsion promotes coexistence of competing species

We propose a new hypothesis for species coexistence by considering behavioral interactions between individuals. The hypothesis states that repulsive behavior between conspecific males (male–male repulsion) creates space for competing species, which promotes their coexistence. This hypothesis can explain the coexistence of two competing species even when their ecological niches completely overlap in spatially homogeneous environments. In addition, the mechanisms underlying such behavior might play a role in enabling the coexistence of two species immediately after speciation, with little or no niche differentiation, as in the case of cichlid fish communities, for example. Although there is limited evidence supporting this hypothesis, it can nevertheless explain the occurrence of species coexistence and biodiversity, which cannot be explained by previous theories.     

The ultimate effect of being cleaned: does ectoparasite removal have reproductive consequences for damselfish clients?

The mutualistic nature of cleaning symbioses has long remainedunconfirmed because of the difficulty in showing net benefitsfor clients. We have previously shown that cleaning gobies (Elacatinusspp.) within territories of Caribbean longfin damselfish (Stegastesdiencaeus) reduce the number of gnathiid isopod ectoparasiteson territory owners. We now investigate whether this benefitof being cleaned has reproductive consequences for male longfindamselfish. The mating success, rate of egg loss, and parentalaggression of 40 nest-guarding males were assessed during sixconsecutive monthly reproductive periods. Ten males had cleaningstations within their territory, 10 males were without cleaningstations, and 20 males initially with a cleaning station hadtheir cleaners removed half-way through the study. Ectoparasiteloads on our focal fish were very low; however, damselfish withcleaning stations still had significantly fewer ectoparasitesthan did fish without cleaning stations. There was, however,no significant difference in the number of eggs, clutches, orarea of clutches received, or in the number of eggs lost beforehatching between damselfish with and without cleaners. We alsofound no difference in parental male aggression between damselfishwith and without cleaners. We conclude that although ectoparasiteremoval appears to have no direct consequence for reproduction,at least for the levels of infestations observed on our studysite, it may still affect other aspects of damselfish fitnesssuch as survival.     

Performance and responses to competition in two congeneric annual species: does seed heteromorphism matter?

Variations in seed characteristics observed in heteromorphic species may affect various stages of their life cycles, e.g. seed dormancy, germination characteristics or even adult plant performance. Highly specialised seed morphs – described as colonisers and maintainers – exhibit a trade‐off between colonisation capacity and competitive traits. The performance of distinct seed morph progeny under competitive conditions, and especially in multi‐species arrangements, had previously not been given much attention. In this study, we compared performance and response to competition among distinct seed morph progenies in two congeneric, co‐occurring species: the invasive Bidens frondosa and the non‐invasive Bidens tripartita. We hypothesised that maintainer seed morphs of both species would perform better under increased plant densities and within inter‐morphic mixtures, while coloniser morphs would show stronger responses to increased densities and perform relatively poorly in inter‐morphic mixtures. We conducted a growth trial and a greenhouse experiment, which revealed that seed morph progeny differed significantly in plant height when grown without competition, while under competitive conditions such differences became less apparent. The observed pattern was more strongly pronounced in B. frondosa, which showed a general predominance in stature and biomass over its non‐invasive congener. Although seed morphs performed equally well under competitive conditions, increased plant height and more rapid germination can favour the maintainer seed morph on sites where vegetation is already present.     

How does spatio-temporal disturbance influence species diversity in a hierarchical competitive system? Prospective order of species coexistence and extinction

To address how habitat destruction and hierarchical competition among species affect the spatio-temporal dynamics of a multi-species community, we present a compartment model in which multiple species undergo dispersal and competitive interactions in a patchy habitat arranged in a two-dimensional lattice. We assume that disturbances are periodically imposed on some parts of the lattice in a block, followed by a period free of disturbance. For convenience, species are ranked in order of competitive ability. We further assume that the intrinsic growth rate of species i, _i , and the dispersal ability, D _i , increase in decreasing order of rank. Our model can analytically determine the exact number of surviving species when disturbance is absent. In the presence of disturbance, we numerically examine how spatio-temporal changes in environmental heterogeneity affect species coexistence and extinction, for the case in which the value of _i /D _i monotonically increases or decreases with rank. The results demonstrate that (1) when the interspecific competition is smaller than the intraspecific competition, we can provide predictions on the prospective order of species to be driven extinct and the order of potential species to revive with increasing extents of disturbance; (2) when the interspecific competition is stronger than intraspecific competition, a small difference in the disturbance level can lead to drastic changes in the species composition, their densities and the order of species extinction. In addition, comparison with other similar models reveals that differences in species interaction in local population dynamics critically affect the disturbance-mediated species diversity.     

Behavioral reproductive isolation among sympatric strains of Brachionus plicatilis Müller 1786: insights into the status of this taxonomic species

We present results on cross-mating experiments using Brachionus plicatilis strains collected in three ponds of a coastal marsh (Torreblanca Marsh, Castellón, Spain). These strains were known to differ widely both in morphology and allozyme patterns from a previous study, where they were grouped into three genetically different clonal groups. Although some of the strains co-occurred in the same pond and sexual periods overlapped, no gene flow was found among them. Our first objective was to determine whether behavioral reproductive isolation was responsible for the absence of interbreeding. A second objective was to explore the relationship between sexual isolation and genetic divergence. We performed two experiments. In Experiment 1, we tested five strains from different clonal groups; in Experiment 2, we added a strain from a congeneric species, and strains from different ponds. We recorded male mating behavior in all possible male-female strain pairings. Our data show that males of a strain tend to mate with females of the same strain or genetically similar strains, regardless of the pond they come from. We also found a high positive correlation between isolation distance and genetic distance. These results support the view that mating behavior acts as an important isolating barrier giving cohesion to clonal groups, and structuring populations of this rotifer, and that Brachionus plicatilis is a taxon composed of more than one biological species.     

When does environmental variation most influence species coexistence?

The ability of environmental variation to affect species coexistence is much studied, yet environmental variation is not always important. I present an approximate calculation for the long-run growth rate of a species in the presence of spatially and temporally correlated environmental variation. I then perform a factorial numerical experiment, varying the mean seed dispersal distances, competition radii, and overwinter seed survival probabilities for two competing species for an array of variational regimes, noting the effects on their long-run growth rates. I find, first, that purely spatial variation has a greater capacity for influence than variation with a temporal component. Second, spatiotemporal variation can promote coexistence as strongly as purely temporal variation or more so, given the right species traits. Third, if the environmental variation has a spatial component, traits which enable species to become spatially segregated promote coexistence most strongly. That is, it is the possibility of spatial segregation which gives spatial variation its large potential to promote coexistence.

Big plants—do they limit species coexistence?

Aims According to conventional theory, larger plant species are likely to inflict more intense competition on other (smaller) species. We tested a deducible prediction from this: that a larger species should generally be expected to impose greater limits on the number of species that can coexist with it.Methods Species richness was sampled under plant canopies for a selection of woody species ('host' species) that display a wide range of adult sizes (from small shrubs to large trees), growing within natural vegetation of the Interior Douglas-fir zone of southern British Columbia, Canada. These data were compared with species richness levels sampled within randomly placed plots within the host species habitat.Important findings A prominent host species size effect on species richness was detected but only narrowly at the small end of the species size range. Across most (90%) of the increasing size range of host species, the number of species residing under the host canopy showed no significant decrease relative to the number expected by random assembly, based on species richness within randomly defined equivalent areas within the habitat of the host species. This apparent 'null effect', we suggest, is explained not because these larger species have no effect on community assembly. We postulate that larger species are indeed likely to be more effective in causing competitive exclusion of some smaller species (as expected from conventional theory), but that any potential limitation effect of this on resident species richness is offset for two reasons: (i) larger species also generate niche spaces that they cannot exploit under their own canopies and so have minimal impact (as competitors) on smaller species that can occupy these niches and (ii) certain other small species—despite small size—have effective competitive abilities under the severe competition that occurs within host neighbourhoods of larger species. These and other recent studies call for re-evaluation of traditional views on the role of plant size in affecting competitive ability and community assembly.     

Diet divergence in two sympatric congeneric butterflies: Community or species level phenomenon?

Summary Two species ofEuphydryas butterflies were studied in California, USA, and showed considerable diet overlap at the species level. They utilize many of the same plant genera for oviposition. However,E. editha is less likely to use woody perennials than isE. chalcedona.Both butterfly species are known to specialize on different host plants in different populations, so species level divergence may not be a good predictor of community level divergence. Within five communities,E. editha andE. chalcedona showed no dietary overlap. A major component of the niche ofE. editha in one community was occupied byE. chalcedona in a second community, even though both butterfly species occupied both communities. These resource use patterns indicate that community level interactions may affect diet divergence. The degree to which divergence within communities is greater (or less) than expected from a species level comparison may be used to provide a measure of community organization. Equations are given in the Appendix for calculating overlap probabilities from presence/absence types of data; in this study, presence is oviposition on a particular plant species, absence is no oviposition on that plant species. Given the various assumptions of the model,E. editha andE. chalcedona show significant community level components of their dietary divergence in the areas studied. However, in some other communitiesE. editha andE. chalcedona do share host plant species. Therefore, we could not demonstrate community level divergence conclusively, nor has this been demonstrated for any other pair of insect herbivore species. We do not know whether this is because the phenomenon is truly rare or just very hard to demonstrate.     

Post-fire mortality and water relations of three congeneric shrub species under extreme water stress — a trade-off with fecundity?

Mortality and water relations of three cooccurringHakea species were studied over the first year following a wildfire in scrub-health in southwestern Australia.Hakea ruscifolia regenerated from both resprouting adults and seedlings, whereasH. smilacifolia andH. polyanthema regenerated only from seedlings. We monitored seedling and resprout survival relative to pre-fire numbers and water relations (shoot water potential, transpiration, pressure-volume parameters) in order to determine the relationship between plant mortality and water relations over the critical first summer drought. Seedlings ofH. polyanthema (few initial seedlings per parent) showed little mortality (8%), achieved through both drought avoidance (low transpiration, high predawn water potential and relative water content (RWC), substantial osmotic adjustment) and drought tolerance later in the season. Seedlings ofH. smilacifolia andH. ruscifolia (high seedling/parent ratios) showed little drought avoidance and high mortality (54–68%). The remaining seedlings spent 3–4 months in a wilted condition (up to 3.6 MPa and 45% RWC below the turgor loss point inH. ruscifolia) indicating marked drought tolerance of the survivors. In contrast to its seedlings,H. ruscifolia resprouts were successful drought avoiders and experienced no mortality. The high level of survival and drought resistance ofH. polyanthema was consistent with its large seedlings (via large seeds) and low initial fecundity. The study highlights the importance of the interaction between ecophysiology-morphology and demography in determining the recruitment strategies of plants.     

Do changes in gene expression contribute to sexual isolation and reinforcement in the house mouse?

Expression divergence, rather than sequence divergence, has been shown to be important in speciation, particularly in the early stages of divergence of traits involved in reproductive isolation. In the two European subspecies of house mice, Mus musculus musculus and Mus musculus domesticus, earlier studies have demonstrated olfactory‐based assortative mate preference in populations close to their hybrid zone. It has been suggested that this behaviour evolved following the recent secondary contact between the two taxa (~3,000 years ago) in response to selection against hybridization. To test for a role of changes in gene expression in the observed behavioural shift, we conducted a RNA sequencing experiment on mouse vomeronasal organs. Key candidate genes for pheromone‐based subspecies recognition, the vomeronasal receptors, are expressed in these organs. Overall patterns of gene expression varied significantly between samples from the two subspecies, with a large number of differentially expressed genes between the two taxa. In contrast, only ~200 genes were found repeatedly differentially expressed between populations within M. m. musculus that did or did not display assortative mate preferences (close to or more distant from the hybrid zone, respectively), with an overrepresentation of genes belonging to vomeronasal receptor family 2. These receptors are known to play a key role in recognition of chemical cues that handle information about genetic identity. Interestingly, four of five of these differentially expressed receptors belong to the same phylogenetic cluster, suggesting specialization of a group of closely related receptors in the recognition of odorant signals that may allow subspecies recognition and assortative mating.     

Immunoglobulin haplotypes: markers of reproductive success?

Immunoglobulin haplotypes are highly polymorphic and are useful for analyses of both macro- and microdifferentiation of populations. The origins of this diversity are not known, but recent reports suggest strong selection at this locus. Increased rates of first-trimester spontaneous abortions have been reported when parents share GM phenotypes. Reduced fertility has been observed in mixed European descent white and Hutterite populations when both parents share immunoglobulin haplotypes. Population samples with completed family information and GM haplotype data are rare; the objective here is to provide this information on another sample. A sample of 242 Mennonite couples with mothers older than 40 years was divided into 3 groups of matings based on how many haplotypes were shared: 0, 1, or 2. The distribution of mean completed family sizes for the three groups were 3.35 +/- 1.85 (n = 23), 3.47 +/- 1.69 (n = 128), and 3.37 +/- 1.60 (n = 91), respectively; these values were not significantly different (F = 0.145, p = 0.865). The log-rank test was used to compare the time-to-next-birth curves. The intervals between first and later births (2-4 births) were not significantly different for the three subgroups either. There is also only limited evidence for segregation distortion in another sample of 923 offspring (in which at least one parent is heterozygous.     

Effects of habitat fragmentation on foraging behaviour of tits and related species: does niche space vary in relation to size and degree of isolation of forest fragments?

We studied the winter foraging niches of tits and related species in deciduous forest fragments varying in size between 1 and 30 ha (plus one forest of 200 ha) in order to investigate the influence of forest fragmentation on foraging niches Very few correlations between niche structure (foraging niche, width and overlap) and forest size or isolation turned out to be significant This implies that either the species that disappear in small fragments are those that suffer most from competition (making the effect unmeasurable), or that competition is relatively unimportant for niche structure In any case we find no evidence that foraging niches are strongly affected by the changes (in habitat and/or community structure) associated with fragmentation     

Body size and species coexistence in consumer–resource interactions: A comparison of two alternative theoretical frameworks

Species coexistence involving trophic interactions has been investigated under two theoretical frameworks—partitioning shared resources and accessing exclusive resources. The influence of body size on coexistence is well studied under the exclusive resources framework, but has received less attention under the shared-resources framework. We investigate body-size-dependent allometric extensions of a classical MacArthur-type model where two consumers compete for two shared resources. The equilibrium coexistence criteria are compared against the general predictions of the alternative framework over exclusive resources. From the asymmetry in body size allometry of resource encounter versus demand our model shows, counterintuitively, and contrary to the exclusive resource framework, that a smaller consumer should be competitively superior across a wide range of supplies of the two resource types. Experimental studies are reviewed to resolve this difference among the two frameworks that arise from their respective assumptions over resource distribution. Another prediction is that the smaller consumer may have relatively stronger control over equilibrium resource abundance, and the loss of smaller consumers from a community may induce relatively stronger trophic cascades. Finally, from satiating consumers’ functional response, our model predicts that greater difference among resource sizes can allow a broader range of consumer body sizes to coexist, and this is consistent with the predictions of the alternative framework over exclusive resources. Overall, this analysis provides an objective comparison of the two alternative approaches to understand species coexistence that have heretofore developed in relative isolation. It advances classical consumer–resource theory to show how body size can be an important factor in resource competition and coexistence.     

Heterogeneity in soil water and light environments and dispersal limitation: what facilitates tree species coexistence in a temperate forest?

In the present study, we analysed the habitat association of tree species in an old‐growth temperate forest across all life stages to test theories on the coexistence of tree species in forest communities. An inventory for trees was implemented at a 6‐ha plot in Ogawa Forest Reserve for adults, juveniles, saplings and seedlings. Volumetric soil water content (SMC) and light levels were measured in 10‐m grids. Relationships between the actual number of stems and environmental variables were determined for 35 major tree species, and the spatial correlations within and among species were analysed. The light level had no statistically significant effect on distribution of saplings and seedlings of any species. In contrast, most species had specific optimal values along the SMC gradient. The optimal values were almost identical in earlier life stages, but were more variable in later life stages among species. However, no effective niche partitioning among the species was apparent even at the adult stage. Furthermore, results of spatial analyses suggest that dispersal limitation was not sufficient to mitigate competition between species. This might result from well‐scattered seed distribution via wind and bird dispersal, as well as conspecific density‐dependent mortality of seeds and seedlings. Thus, both niche partitioning and dispersal limitation appeared less important for facilitating coexistence of species within this forest than expected in tropical forests. The tree species assembly in this temperate forest might be controlled through a neutral process at the spatial scale tested in this study.     

Are tetraploids more successful? Floral signals,reproductive success and floral isolation in mixed-ploidy populations of a terrestrial orchid

Background and Aims Polyploidization, the doubling of chromosome sets, is common in angiosperms and has a range of evolutionary consequences. Newly formed polyploid lineages are reproductively isolated from their diploid progenitors due to triploid sterility, but also prone to extinction because compatible mating partners are rare. Models have suggested that assortative mating and increased reproductive fitness play a key role in the successful establishment and persistence of polyploids. However, little is known about these factors in natural mixed-ploidy populations. This study investigated floral traits that can affect pollinator attraction and efficiency, as well as reproductive success in diploid and tetraploid Gymnadenia conopsea (Orchidaceae) plants in two natural, mixed-ploidy populations.Methods Ploidy levels were determined using flow cytometry, and flowering phenology and herbivory were also assessed. Reproductive success was determined by counting fruits and viable seeds of marked plants. Pollinator-mediated floral isolation was measured using experimental arrays, with pollen flow tracked by means of staining pollinia with histological dye.Key Results Tetraploids had larger floral displays and different floral scent bouquets than diploids, but cytotypes differed only slightly in floral colour. Significant floral isolation was found between the two cytotypes. Flowering phenology of the two cytotypes greatly overlapped, and herbivory did not differ between cytotypes or was lower in tetraploids. In addition, tetraploids had higher reproductive success compared with diploids.Conclusions The results suggest that floral isolation and increased reproductive success of polyploids may help to explain their successful persistence in mixed-ploidy populations. These factors might even initiate transformation of populations from pure diploid to pure tetraploid.