The contribution of multiple barriers to reproduction between edaphically divergent lineages in the Amazonian tree Protium subserratum (Burseraceae)

Disentangling the strength and importance of barriers to reproduction that arise between diverging lineages is central to our understanding of species origin and maintenance. To date, the vast majority of studies investigating the importance of different barriers to reproduction in plants have focused on short‐lived temperate taxa while studies of reproductive isolation in trees and tropical taxa are rare. Here, we systematically examine multiple barriers to reproduction in an Amazonian tree, Protium subserratum (Burseraceae) with diverging lineages of soil specialist ecotypes. Using observational, molecular, distributional, and experimental data, we aimed to quantify the contributions of individual prezygotic and postzygotic barriers including ecogeographic isolation, flowering phenology, pollinator assemblage, pollen adhesion, pollen germination, pollen tube growth, seed development, and hybrid fitness to total reproductive isolation between the ecotypes. We were able to identify five potential barriers to reproduction including ecogeographic isolation, phenological differences, differences in pollinator assemblages, differential pollen adhesion, and low levels of hybrid seed development. We demonstrate that ecogeographic isolation is a strong and that a combination of intrinsic and extrinsic prezygotic and postzygotic barriers may be acting to maintain near complete reproductive isolation between edaphically divergent populations of the tropical tree, P. subserratum.     

Methodological considerations for examining the relationship between sperm morphology and motility

Sperm cells of all taxa share a common goal to reach and fertilize an ovum, yet sperm are one of the most diverse cell types in nature. While the structural diversity of these cells is well recognized, the functional significance of variation in sperm design remains elusive. An important function of spermatozoa is a need to migrate toward the ova, often over long distances in a foreign environment, which may include a complex and hostile female reproductive tract. Several comparative and experimental studies have attempted to address the link between sperm morphology and motility, yet the conclusions drawn from these studies are often inconsistent, even within the same taxa. Much of what we know about the functional significance of sperm design in internally fertilizing species has been gleaned from in vitro studies, for which experimental parameters often vary among studies. We propose that discordant results from these studies are in part due to a lack of consistency of methods, conditions that do not replicate those of the female reproductive tract, and the overuse of simple linear measures of sperm shape. Within this review, we provide a toolkit for imaging, quantifying, and analyzing sperm morphology and movement patterns for in vitro studies and discuss emerging approaches. Results from studies linking morphology to motility enhance our understanding of the evolution of adaptive sperm traits and the mechanisms that regulate fertility, thus offering new insights into methods used in assisted reproductive technologies in animal science, conservation and public health.     

REPRODUCTIVE BIOLOGY OF ERYTHRONIUM GRANDIFLORUM VARIETIES GRANDIFLORUM AND CANDIDUM (LILIACEAE)

This four-year (1982–1986) study compared the pollination biology and cytology of a relatively rare taxon, Erythronium grandiflorum Pursh var. candidum (Piper) Abrams, with that of a geographically widespread sister taxon, E. grandiflorum var. grandiflorum, in the Pacific Northwest. Breeding studies were used to study the reproductive systems of the taxa, to test for interfertility between them, and to seek abnormalities in the breeding system of the rare taxon that might account for its relative rarity. Chromosomes were counted in both taxa and in hybrids from artificial crosses. Ranges of the two taxa were determined from field studies and herbarium specimens. Although the ranges of the taxa overlap in part, populations are usually allopatric. Phenological factors are probably minor in preventing cross-pollination between the taxa. Both taxa are protogynous obligate outcrossers pollinated by bees. Seed production apparently is not pollinator-limited. The two taxa are interfertile only when individuals from allopatric populations are artificially crossed, and thus should be considered two biological species. When the taxa overlap in floral phenology in sympatric populations, they exhibit reciprocal incompatibility. Such incompatibility between closely related perennial species is unusual. It may have arisen via natural selection in mixed populations. Alternatively, if populations of each taxon vary with regard to their incompatibility alleles, they may have acquired their fertility barriers by chance before populations of the two taxa came into contact with each other.     

Growth and reproduction of New Zealand

In New Zealand, as elsewhere, research on rare species has been dominated by autecological studies of individual threatened species. Limitations of this approach are that it involves no comparison with related common species which may have similar traits, and that the minimal sample size prevents generalisation about causes and consequences of rarity. We report on experimentally determined growth and reproductive traits of 10 rare and common Acaena(Rosaceae) species from two taxonomic sections (sect. Ancistrum and sect. Microphyllae). We examined the relationship between rarity or commonness and relative growth rate, mode of vegetative expansion, morphology/presentation of reproductive structures and reproductive allocation. Rarity and commonness were defined according to geographic range size, measured as the number of 10-km grid squares containing at least one record of the species. There were tendencies across both taxonomic sections for species with large range size to have higher relative growth rates and in section Microphyllae, faster lateral expansion. Among section Ancistrum species, common species tended to produce inflorescences for a shorter period and held their capitula higher above the canopy, but other reproductive attributes showed little association with range size. In section Microphyllae all reproductive traits tended to be positively associated with range size. This was mainly due to the single very common species having high fecundity. The lack of strong patterns among our results may reflect insufficient sample size or that the rare species represent different types of rarity.     

Brood rearing costs affect future reproduction in the precocial common goldeneye Bucephala clangula

Life-history theory assumes a trade-off between current reproductive effort and future reproductive success. There are a large number of studies demonstrating reproductive trade-offs in different animal taxa, particularly in birds. Most bird studies have focused on the costs of chick rearing in altricial species. These costs have been assumed to be low in precocial species, but this aspect has been little studied. We used long-term individual reproductive data from the common goldeneye Bucephala clangula , an iteroparous precocial duck with uniparental female care, to examine whether brood rearing carries costs that affect future reproductive performance. All females were experienced breeders, and possible differences in female quality were ruled out. We compared within-individual (between-year) changes in clutch size, hatching date and body mass between females that had reared a brood in the previous year and females that had not. It turned out that brood rearing involved a cost in terms of clutch size and hatching date the next year, but not in terms of body mass: females that had reared a brood in the previous year laid relatively smaller clutches and laid relatively later than females that had not reared a brood. Our results show that normal brood rearing in a precocial species involves costs that affect future reproduction.     

Are rare primate taxa specialists or simply less studied?

Aim Rare species are reported to be specialized. However, rare taxa are usually less studied than are common taxa. If so, the reported specialization might be just a result of paucity of records. We here test for this sampling artefact in primates, a taxon in which rarity has been explained by specialization. Location Tropical Africa, Madagascar, Asia, Americas. Methods We define rare and common species as those with geographical range sizes in the lower and upper quartiles, respectively, for primates in each realm. We conducted two independent searches of published literature to determine if there were significantly fewer studies on a common measure of specialization, diet, for rare vs. common species. We then tested for sampling artefact in reported diet breadth by comparing the number of references needed to obtain it for both rare and common species. Results We found, in both literature searches, significantly fewer studies on diet for rare primates – a mode of zero references for rare species, and one for common. By contrast, no significant difference existed for number of references needed to attain the full reported diet breadth: a median of one reference for both specialized, rare and generalized, common species. Main conclusions Rare species are indeed studied less. Nevertheless, the finding that rare primates are specialists is not necessarily mere sampling artefact.     

The effect of excluding taxa with low abundances or taxa with small distribution ranges on ecological assessment

The present study aims to investigate whether taxa with a small distribution range or taxa with low abundances indicate specific habitats or a high ecological quality and what the effect is if these taxa are excluded from ecological assessment. We compared autecological features between stream dwelling taxa with a mean abundance >5 individuals per sample and a mean abundance ≤5 individuals per sample as well as between taxa with a small distribution range and taxa with a large distribution range. The number of rare taxa (either with a small distribution range or with low abundances) in a sample was related to the ecological quality classes. To test the effect of exclusion of rare taxa we constructed 8 data sets all including 142 samples of Dutch lowland streams. From each data set we stepwise excluded taxa that had low abundances or taxa that were known to be restricted in their distribution range. With help of the AQEM assessment software we calculated the final ecological quality classes and the metrics that were included in the multimetric for the original data and the 8 selected data sets. Autecological features of the taxa within the different selections showed that taxa with small distribution ranges were often running water taxa, living on stones and gravel and indicating oligosaprobic water conditions in contrast to taxa that had a large distribution range. There were only small differences between taxa with low and high abundances. However, current velocity preference was lower for taxa with abundance ≤5 individuals per sample, saprobic values were higher and scores for typical stream habitats, such as lithal, psammal and akal were lower compared to high abundant taxa. If taxa with low abundances were excluded a higher ecological quality class was achieved in most cases, while excluding taxa with a small distribution range resulted in lower ecological quality classes. In conclusion, excluding taxa with a small distribution range led to worse ecological quality classes because these taxa have special autecological features that often indicate natural streams. On the other hand, excluding taxa with low abundances resulted in higher ecological quality classes because these taxa indicate more disturbed situations and because the number of taxa per sample was strongly reduced. Although the documentation of rare taxa (either with low abundances or with small distribution ranges) is often time and cost-intensive regarding field work, laboratory work, data processing, and analyses, the indicative power of these taxa for natural circumstances is essential and therefore rare taxa should be included in ecological assessment studies.     

Life history tactics of darters (Percidae: Etheostomatiini) and their relationship with body size, reproductive behaviour, latitude and rarity

Patterns of covariation of life history traits of darters in the genus Etheostoma are reviewed. The primary pattern is associated with body size. Large darters grow faster, mature at a larger size, produce bigger clutches, and have longer reproductive and life spans, and shorter spawning seasons, than do small darters. When the effects of size are removed statistically, the dominant secondary pattern matched the r-K continuum from fast-growing, short-lived, primarily semelparous species with many small ova and a high reproductive effort (r-species) to slow-growing, long-lived, iteroparous species with few large ova and a low reproductive effort (K-species). Variation in life history traits is also influenced by reproductive behaviour, latitude, and rarity (as measured by geographic range). There are significant differences in the primary and secondary life history patterns among reproductive guilds. Latitude and rarity are not correlated with these primary and secondary patterns. Instead, they account for variation of tertiary patterns. Rare species may not match the reproductive performance of more common and widely distributed species. Future studies of life history traits in darters should focus on species whose reproductive behaviour differs from that of the species reviewed in this study, and on the demographic characteristics of rare or declining populations.     

Divergent host plant adaptation and reproductive isolation between ecotypes of Timema cristinae walking sticks

Theoretical and empirical studies have demonstrated that divergent natural selection can promote the evolution of reproductive isolation. Three unresolved questions concern the types of reproductive barriers involved, the role of geography, and the factors determining the extent of progress toward complete speciation. Here I synthesize studies of Timema cristinae host plant ecotypes to address these issues. The approach is to compare the magnitude of multiple reproductive barriers among different ecological and geographic scenarios, where pairs of populations within each scenario are the unit of replication. Application of this approach to T. cristinae revealed that divergent host adaptation can promote the evolution of diverse reproductive barriers, including those that are not inherently ecological. Gene flow in parapatry tended to constrain divergence, with the notable exception of the reinforcement of sexual isolation. Thus, geography affected progress toward speciation but did not influence all reproductive barriers in the same way. Studies of any single pair of taxa often capture only certain stages of the speciation process. For example, reproductive isolation between T. cristinae ecotypes is incomplete, and so only the stages before the completion of speciation have been examined. Studies of more divergent taxa within the genus are required to determine the factors that complete speciation.     

Better common than rare? Effects of low reproductive success,scarce pollinator visits and interspecific gene flow in threatened and common species of Tibouchina (Melastomataceae)

The reasons for plant rarity have been the focus of many studies, especially because rare species are more prone to extinction than common species. Under the same habitat conditions, rare plants are expected to attract fewer flower visitors and to show some limitation in their reproductive success. Here, using one of the most emblematic Neotropical plant genus (Tibouchina) we tested whether narrow endemic and threatened species in Ecuador have a lower reproductive success or are visited by fewer pollinators than common species, in 13 populations monitored from 2011 to 2013. We also assessed whether interspecific gene flow could be considered a threat to the rare species. However, contrary to expectations, we found that few pollinators visited the flowers, independently of species rarity. Natural outcross pollinations were always very low in all small‐size populations, leading to high levels of pollen limitation. Interspecific crossing experiments also revealed weak reproductive barriers in some species. This study reveals that both narrow and common species of Tibouchina have similar reproductive and pollinator patterns in Ecuador and, therefore, other causes of the rarity of these species should be considered.     

Co-occurrence patterns of common and rare leaf-litter frogs, epiphytic ferns and dung beetles across a gradient of human disturbance

Indicator taxa are commonly used to identify priority areas for conservation or to measure biological responses to environmental change. Despite their widespread use, there is no general consensus about the ability of indicator taxa to predict wider trends in biodiversity. Many studies have focused on large-scale patterns of species co-occurrence to identify areas of high biodiversity, threat or endemism, but there is much less information about patterns of species co-occurrence at local scales. In this study, we assess fine-scale co-occurrence patterns of three indicator taxa (epiphytic ferns, leaf litter frogs and dung beetles) across a remotely sensed gradient of human disturbance in the Ecuadorian Amazon. We measure the relative contribution of rare and common species to patterns of total richness in each taxon and determine the ability of common and rare species to act as surrogate measures of human disturbance and each other. We find that the species richness of indicator taxa changed across the human disturbance gradient but that the response differed among taxa, and between rare and common species. Although we find several patterns of co-occurrence, these patterns differed between common and rare species. Despite showing complex patterns of species co-occurrence, our results suggest that species or taxa can act as reliable indicators of each other but that this relationship must be established and not assumed.     

Rarity in the tropics: biogeography and macroecology of the primates

Aim To describe rarity and elucidate its biology in a tropical mammalian order, the Primates. Location Africa, Central and South America, Asia, Madagascar. Methods A review of the literature, with some additional analyses using data from the literature. A variety of definitions of rarity are used in order to describe it and to investigate its biology by correlating the degree of rarity with a variety of biological traits indicative of resource use (e.g. size of annual home range), reproductive rate (e.g. birth interval)and specialization (e.g. number of habitat types used). Results Few primate taxa occur outside the tropics, and most taxa are rare (small geographical range size or latitudinal extent, low density or both). Latitudinal extent is narrower at lower latitudes in Africa and Asia, but the potential resultant packing of taxa appears not to explain the taxonomic diversity gradient. Whilst primate species do not show the common, positive density by range size relationship, primate genera show a significant shallow slope, and primate families/subfamilies a strongly positive slope. Rare taxa are specialized, but neither use more resources nor breed more slowly than common taxa. The correlation of rarity and specialization is via geographical range: taxa with small ranges, or small ranges for their density, are specialized, but not taxa at low density. Common taxa are generalized because they consist of more differently specialized subtaxa, not because each subtaxon is generalized. Main conclusions Most primate taxa are rare, in which case most are presumably likely to go extinct. Rare primates are specialized, but do not necessarily use more resources, nor breed more slowly. Specialization as an explanation for rarity appears to work via constriction of range size, not of density. Common primates might be common (large range size) not because subtaxa or individuals are generalized, but because they are composed of more subtaxa. A consequence could be that persistence of even common taxa will depend on conservation of several populations scattered across the taxon's geographical range.     

Reproductive mode may determine geographic distributions in Australian venomous snakes (Pseudechis,Elapidae)

Summary Why are viviparous squamate reptiles more common in cold climates, and oviparous ones in warmer areas? The usual explanation is that (1) oviparous squamates cannot reproduce successfully in cold areas because soil temperatures are too low for embryonic development; and (2) viviparous squamates experience lower survivorship or reproductive success than oviparous taxa in warmer areas. These hypotheses suggest that the boundaries of geographic distributions of congeneric oviparous and viviparous squamates should be predictable from data on thermal tolerances of embryos, and estimated temperatures of soils and gravid female reptiles throughout the potential geographic range of the taxon. In large venomous Australian snakes of the genus Pseudechis, distributional boundaries of oviparous and viviparous taxa can be accurately predicted from such data. This predictive ability, if substantiated by studies of other reproductively biomodal squamate taxa, would support the putative role of reproductive mode as a direct determinant of reptilian geographic distributions.     

Determinants of species rarity: population growth rates of species sharing the same habitat

Determining differences between common and rare species is commonly used to identify factors responsible for rarity. Existing studies, however, suffer from two important drawbacks. First, studies compare species that are closely related phylogenetically but occupy different habitats. Second, these studies concentrate on single life history traits, with unknown relevance for population growth rates. Complete life cycles of one rare and one common Cirsium species sharing the same habitat were compared. Population growth rate was slightly lower in the rare species, translating into a large difference in local extinction probability. Seed predation intensity did not differ between species. However, it can be demonstrated that in connection with the data on complete demography, seed predation is the key factor causing a lower population growth rate in the rare species. These results are the first estimation of factors responsible for commonness or rarity of plants in terms of population growth rate without confounding differences in ecology. They demonstrate that conclusions based on single traits may be misleading and that only a comparison based on a complete life cycle can provide unequivocal evidence for concluding which factors are really those responsible for species commonness or rarity.     

Quantifying patterns in the evolution of reproductive isolation

We present a likelihood-based statistical method for examining the pattern or rate of evolution of reproductive isolation. The method uses large empirical datasets to estimate, for a given clade, the average duration of two phases in the divergence of populations. The first phase is a lag phase and refers to the period during which lineages diverge but no detectable reproductive isolation evolves. The second is an accumulation phase, referring to the period during which the magnitude of reproductive isolation between diverging lineages increases. The pattern of evolution is inferred from the relative durations of these two phases. Results of analyses of postzygotic isolation data indicate significant differences among taxa in the pattern of evolution of postzygotic isolation that are consistent with predictions based on genetic differences among these groups. We also examine whether the evolution of postzygotic isolation is best explained by either of two models for the rate of accumulation: a linear model or a quadratic function as may be suggested by recent studies. Our analysis indicates that the appropriateness of either model varies among taxa.     

Electrophoretic delineation of species boundaries within the short-necked freshwater turtles of Australia (Testudines: Ghelidae)

A total of 222 specimens from 55 populations of short-necked chelid turtle was collected from drainages in Australia and Papua New Guinea. Two populations were initially considered to belong to different diagnosable taxa if all individuals in one population could be distinguished from all individuals in the other by fixed allozyme differences. When two populations or diagnosable taxa shared allozymes at all presumptive loci, their profiles were combined into a single diagnosable taxon. Comparisons between populations and emerging diagnosable taxa were repeated until no further changes were possible. The species Elseya dentata comprised five clearly diagnosable taxa, differing by between 4 and 19 fixed allozyme differences. The currently recognized El. latisternum and El. novaeguineae were each a single diagnosable taxon, and there were three diagnosable taxa, including a sibling pair, that could not be assigned to a currendy described Elseya species. In contrast, all forms of Emydura were very closely related, with no two taxa differing by more than three fixed allozyme differences. There were three diagnosable taxa in the north (Em. victoriae, Em. subglobosa and one new form), though support for them was marginal. In the south, Em. macquarii, Em. krefflii and Em. signata formed only a single diagnosable taxon, even sharing rare alleles. If the phylogenetic species concept is adopted, there is support for recognition of 16 species of short-necked turtle in Australia, including Pseudemydura umbrina. Currendy only 10 are described. Our data also provide evidence of reproductive isolation in some cases (sympatric or parapatric), and comparative evidence (sensu Mayr) in others, than the traditional biological species concept applies also to these diagnosable taxa.     

Challenges in estimating past plant diversity from fossil pollen data: statistical assessment, problems, and possible solutions

Fossil pollen data from sediment cores may be used as a measure for past plant diversity. According to the theory of probability, palynological richness is positively related to the pollen count. In a low pollen count, only common taxa are detected, whereas rare taxa are only detected by chance. The detection of all pollen taxa requires a very high pollen count, which is time-consuming. In regular palynological investigations, the detected richness in pollen spectra varies with the pollen count. Rarefaction analysis estimates palynological richness in an exactly equal-sum count for all samples, so that comparison between samples is meaningful. However, the over-representation of some taxa suppresses the detection probability of rare taxa; low total pollen abundance in a sample enhances the detection probability of rare taxa and long-distance transported pollen grains. These factors bias the observed palynological richness and distort comparisons. Palynological richness in a pollen count proportional to its pollen influx may be one proxy for reconstructing diversity trends through time. The use of this proxy overcomes most problems encountered in rarefaction analysis, but is constrained by inaccuracy in estimating pollen influx due to the imprecise time control of sediment cores. Estimating palynological richness by mathematical methods may be another way of reconstructing pollen diversity. Pollen data tend to reflect diversity on a regional scale. Sites from small basins have the advantage of recording diversity at both local and regional scales, if the detection of each taxon is independent. By associating one site from a large basin with a series of sites from very small basins (e.g. forest-hollows), information about both regional and local diversity may be obtained. Entomophilous pollen taxa may have to be measured using a different strategy than anemophilous taxa.     

BIOLOGICAL AND HISTORICAL FACTORS INFLUENCING GENETIC DIVERSITY IN THE SCUTELLARIA ANGUSTIFOLIA COMPLEX (LABIATAE)

Studies of genetic diversity at isozyme loci were used to examine the phylogenetic distribution of several frequently reported population-genetic parameters in a putatively monophyletic group of plant species, the Scutellaria angustifolia complex. The influence of taxon-specific differences in habitat preference, breeding system, degree of endemism, and phylogenetic relatedness was examined. Many characters of reproductive morphology traditionally used in phylogenetic inference vary with breeding system. To the extent that reproductive systems are conservative markers of phylogenetic relationships, one would expect the distribution of genetic variation to be similar in closely related taxa. Results showed that closely related taxa may exhibit very different genetic-diversity statistics and that distantly related taxa may exhibit very similar genetic-diversity statistics. This suggests that complex patterns of evolution of breeding systems and morphological characters have occurred in the ten taxa included in the Scutellaria angustifolia complex. Similarity in habitat is not associated with similarity in genetic diversity in this group of species.     

Competition and predation as possible causes of bacterial rarity

We assembled communities of bacteria and exposed them to different nutrient concentrations with or without predation by protists. Taxa that were rare in the field were less abundant at low nutrient concentrations than common taxa, independent of predation. However, some taxa that were rare in the field became highly abundant in the assembled communities, especially under ample nutrient availability. This high abundance points at a possible competitive advantage of some rare bacterial taxa under nutrient-rich conditions. In contrast, the abundance of most rare bacterial taxa decreased at low resource availability. Since low resource availability will be the prevailing situation in most soils, our data suggests that under those conditions poor competitiveness for limiting resources may contribute to bacterial rarity. Interestingly, taxa that were rare in the field and most successful under predator-free conditions in the lab also tended to be more reduced by predation than common taxa. This suggests that predation contributes to rarity of bacterial taxa in the field. We further discuss whether there may be a trade-off between competitiveness and predation resistance. The substantial variability among taxa in their responses to competition and predation suggests that other factors, for example abiotic conditions and dispersal ability, also influence the local abundance of soil bacteria.     

The role of allochrony in speciation

The importance of sympatric speciation – the evolution of reproductive isolation between codistributed conspecific individuals – in generating biodiversity is highly controversial. Allochrony, or differences in breeding time (phenology) between conspecific individuals, has the potential to lead to reproductive isolation and therefore speciation. We critically review the literature to test the importance of allochronic speciation over the three timescales over which allochrony can occur – over the day, between seasons or between years – and explore what is known about genomic mechanisms underlying allochrony in the diverse taxa in which it is found. We found that allochrony can be a key contributor to reproductive isolation, especially if populations have little overlap in breeding time and therefore little potential for gene flow, and may sometimes be the initial or key driver of speciation. Shifts in phenology can be caused by several factors, including a new ecological opportunity, environmental change, or reinforcement. The underlying genomic basis of allochrony has been studied mostly in insects, highlighting the need for genomic studies in other taxa; nonetheless, results to date indicate that several cases of allochrony involve changes in circadian genes. This review provides the first comprehensive discussion of the role of allochrony in speciation and demonstrates that allochrony as a contributor to divergence may be more widespread than previously thought. Understanding genomic changes and adaptations allowing organisms to breed at new times may be key in the light of phenological changes required under climate change.