Sex‐specific floral attraction traits in a sequentially hermaphroditic species

• ● Many angiosperms are hermaphroditic and produce bisexual flowers in which male (pollen export) and female (stigma receptivity) functions are separated temporally. This sequential hermaphroditism may be associated with variation in flower size, color, or pattern, all of which may influence pollinator attraction. In this study, we describe variation in these traits across discrete functional sex stages within and between 225 greenhouse‐grown individuals of Clarkia unguiculata (Onagraceae). In addition, to identify the effects of floral phenotype on pollinator attraction in this species, we examine the effects of these floral traits on pollen receipt in ~180 individuals in an experimental field array.
• ● Petal area, ultraviolet (UV)‐absorbing nectar guide area, and blue and green mean petal reflectance differ significantly across the functional sex stages of C. unguiculata. Male‐ and female‐phase flowers display significantly different pollinator attraction traits. Petal and UV nectar guide area increase as flowers progress from male phase to female phase, while blue reflectance and green reflectance peak during anther maturation.
• ● In field arrays of C. unguiculata, female‐phase flowers with large UV nectar guides receive more pollen than those with small nectar guides, and female‐phase flowers with high mean blue reflectance values are more likely to receive pollen than those with low blue reflectance. Female‐phase flowers with green mean reflectance values that differ most from background foliage also receive more pollen than those that are more similar to foliage. These findings indicate that components of flower color and pattern influence pollen receipt, independent of other plant attributes that may covary with floral traits. We discuss these results in the context of hypotheses that have been proposed to explain sex‐specific floral attraction traits, and we suggest future research that could improve our understanding of sexual dimorphism in sequentially hermaphroditic species and the evolution of features that promote outcrossing.

     

Morph‐specific selection on floral traits in a polymorphic plant

Correlations between phenotypic traits are common in many organisms, but the relative importance of nonadaptive mechanisms and selection for the evolution and maintenance of such correlations are poorly understood. In polymorphic species, morphs may evolve quantitative differences in additional characters as a result of morph‐specific selection. The perennial rosette herb Primula farinosa is polymorphic for scape length. The short‐scaped morph is less damaged by grazers and seed predators but is more strongly pollen limited than the long‐scaped morph. We examined whether morph‐specific differences in biotic interactions are associated with differences in selection on two other traits affecting floral display (number of flowers and petal size) and on one trait likely to affect pollination efficiency (corolla tube width) in three P. farinosa populations. Differences in selection between morphs were detected in one population. In this population, selection for more flowers and larger petals was stronger in the short‐scaped than in the long‐scaped morph, and although there was selection for narrower corolla tubes in the short‐scaped morph, no statistically significant selection on corolla tube width could be detected in the long‐scaped morph. In the study populations, the short‐scaped morph produced more and larger flowers and wider corolla tubes. Current morph‐specific selection was thus only partly consistent with trait differences between morphs. The results provide evidence of morph‐specific selection on traits associated with floral display and pollination efficiency, respectively.     

Total annual seed loss on a perennial legume through predation by insects: The importance of within‐season seed and seed feeder dynamics

Abstract Determining total annual seed loss from seed predators is an important step in quantifying the role they have in modifying plant populations. Total seed loss is typically estimated with a single, well‐timed survey. However, this overlooks the potential importance of within‐season patterns of seed availability and insect activity, particularly where seed gain and loss are not synchronous and where insects are multivoltine. In Australia the introduced legume weed, Parkinsonia aculeata L. (Caesalpinaceae) is one such example. A replicated survey was conducted throughout a single cropping season in two contrasting habitats (uplands and wetland) to estimate total annual seed loss from seed predation and to test the relative importance of seed availability, seed feeder abundance, seed feeder behaviour and parasitism in determining total seed loss. Two seed feeders were present, the introduced biological control agent Penthobruchus germaini (Pic) (Bruchidae) and the moth, Mesophleps palpigera (Walsingham) (Gelechiidae). Seed availability patterns differed with habitat, with a greater proportion of seeds being available for longer in uplands, and resulted in total seed consumption by the beetle being twice as high in the uplands (5.2%) and no difference between habitats for the moth. Total seed loss from beetle predation was restricted by the egg parasitoid Uscana sp. (Trichogrammatidae), which was abundant throughout the season, and also by unexplained larval mortalities. This study highlights the potential importance of within‐season interactions between plant, seed feeder, natural enemies and environment in determining total seed loss through predation. The possible population and evolutionary consequences of such interactions for both the plant and the seed feeder require further consideration.     

Sex‐specific selection and sexual size dimorphism in the waterstrider Aquarius remigis

We estimated selection on adult body size for two generations in two populations of Aquarius remigis, as part of a long‐term study of the adaptive significance of sexual size dimorphism (SSD). Net adult fitness was estimated from the following components: prereproductive survival, daily reproductive success (mating frequency or fecundity), and reproductive lifespan. Standardized selection gradients were estimated for total length and for thorax, abdomen, genital and mesofemur lengths. Although selection was generally weak and showed significant temporal and spatial heterogeneity, patterns were consistent with SSD. Prereproductive survival was strongly influenced by date of eclosion, but size (thorax and genital lengths in females; total and abdomen lengths in males) played a significant secondary role. Sexual selection favoured smaller males with longer external genitalia in one population. Net adult fitness was not significantly related to body size in females, but was negatively related to size (thorax and total length) in males.     

Phenotypic selection on floral traits in the arctic plant Parrya nudicaulis (Brassicaceae)

The evolution of floral traits is often attributed to pollinator‐mediated selection; however, the importance of pollinators as selective agents in arctic environments is poorly resolved. In arctic and subarctic regions that are thought to be pollen limited, selection is expected to either favor floral traits that increase pollinator attraction or promote reproductive assurance through selfing. We quantified phenotypic selection on floral traits in two arctic and two subarctic populations of the self‐compatible, but largely pollinator‐dependent, Parrya nudicaulis. Additionally, we measured selection in plants in both open pollination and pollen augmentation treatments to estimate selection imposed by pollinators in one population. Seed production was found to be limited by pollen availability and strong directional selection on flower number was observed. We did not detect consistently greater magnitudes of selection on floral traits in the arctic relative to the subarctic populations. Directional selection for more pigmented flowers in one arctic population was observed, however. In some populations, selection on flower color was found to interact with other traits. We did not detect consistently stronger selection gradients across all traits for plants exposed to pollinator selection relative to those in the pollen augmentation treatment; however, directional selection tended to be higher for some floral traits in open‐pollinated plants.     

Characterization of animal communities involved in seed dispersal and predation of Guibourtia tessmannii (Harms) J.Léonard,a species newly listed on Appendix II of CITES

Characterization of the ecology of endangered timber species is a crucial step in any forest management strategy. In this study, we described the animal communities involved in seed dispersal and predation of a high‐value timber species Guibourtia tessmannii (Fabaceae; Detarioideae), which is newly listed on Appendix II of CITES. We compared the animal communities between two forest sites (Bambidie in Gabon and Ma'an in Cameroon). A total of 101 hr of direct observations and 355 days of camera trapping revealed that a primate (Cercopithecus nictitans nictitans) and a hornbill (Ceratogymna atrata) were important seed dispersers in Gabon. Conversely, a greater presence of a rodent (Cricetomys emini), which could act both as predator and disperser, was observed in Cameroon. This study suggests that animal communities involved in seed dispersal of G. tessmannii may vary depending on environmental conditions and anthropogenic impacts. However, further studies are needed to properly identify the factors involved in seed dispersal and predation of G. tessmannii.     

Sex‐specific selection on plant architecture through “budget” and “direct” effects in experimental populations of the wind‐pollinated herb,Mercurialis annua

Sexual selection may contribute to the evolution of plant sexual dimorphism by favoring architectural traits in males that improve pollen dispersal to mates. In both sexes, larger individuals may be favored by allowing the allocation of more resources to gamete production (a “budget” effect of size). In wind‐pollinated plants, large size may also benefit males by allowing the liberation of pollen from a greater height, fostering its dispersal (a “direct” effect of size). To assess these effects and their implications for trait selection, we measured selection on plant morphology in both males and females of the wind‐pollinated dioecious herb Mercurialis annua in two separate experimental common gardens at contrasting density. In both gardens, selection strongly favored males that disperse their pollen further. Selection for pollen production was observed in the high‐density garden only, and was weak. In addition, male morphologies associated with increased mean pollen dispersal differed between the two gardens, as elongated branches were favored in the high‐density garden, whereas shorter plants with longer inflorescence stalks were favored in the low‐density garden. Larger females were selected in both gardens. Our results point to the importance of both a direct effect of selection on male traits that affect pollen dispersal, and, to a lesser extent, a budget effect of selection on pollen production.     

Testing the quick meal hypothesis: The effect of pulp on hoarding and seed predation of Hymenaea courbaril by red‐rumped agoutis (Dasyprocta leporina)

Abstract: Red‐rumped agoutis (Dasyprocta leporina) are important seed dispersers/predators of Neotropical large‐seeded plants. Several species of seeds cached by agoutis have an edible reward, in contrast to temperate rodent‐dispersed diaspores. The quick meal hypothesis states that the presence of a reward such as edible pulp will enhance the efficiency of rodents as seed disperses by satiating the animal and, consequently, reducing seed predation and enhancing hoarding. In this study, this hypothesis was tested using as the reference system the pulp and seeds of Hymenaea courbaril. Seeds with and without pulp were offered to agoutis and the behaviour of each individual was recorded. Since the probability of predation and hoarding were complementary, we used the probability of predation. The proportion of agoutis that preyed on at least one seed was similar for seeds with (42.8% of individuals) and without (40.0% of individuals) pulp. In agoutis that preyed upon at least one seed, the probability that they killed a seed did not differ between seeds with (0.17 ± 0.03) and without (0.20 ± 0.08) pulp. Hence, these results do not support the ‘quick meal hypothesis’.     

Decorative sterile flowers in nine Japanese species of Viburnum (Adoxaceae) and their influence on pollinator visits

Framed inflorescences are unique arrangements in which a cluster of small fertile flowers is surrounded by several larger, decorative sterile flowers. Viburnum (Adoxaceae) species vary in their inflorescence arrangements; some species exhibit framed inflorescences, whereas others do not. We hypothesize that the decorative flowers increase the pollinator-attracting functions of the inflorescences; as proved by previous studies, they additionally function as landing-sites for pollinators. To test our hypotheses, field manipulation experiments were carried out for nine Viburnum species, three with inherently framed inflorescences and six without them: sterile flowers were removed and mounted on species with and without framed inflorescences, respectively. Results show that inflorescences with decorative flowers had higher visit rates than inflorescences without them, and that insect flower visitors did not show landing preference for either flower type. These results suggest that decorative flowers appeared only in a subset of Viburnum species to increase their pollination chances by, mainly, enhancing the attractiveness of the inflorescence. It is likely that species without framed inflorescences use other attraction-enhancing mechanisms, such as a high flowering synchrony within a single cluster of fertile flowers, a trait found in most studied species without decorative flowers.     

Sex‐specific mitonuclear epistasis and the evolution of mitochondrial bioenergetics,ageing, and life history in seed beetles

The role of mitochondrial DNA for the evolution of life‐history traits remains debated. We examined mitonuclear effects on the activity of the multisubunit complex of the electron transport chain (ETC) involved in oxidative phosphorylation (OXPHOS) across lines of the seed beetle Acanthoscelides obtectus selected for a short (E) or a long (L) life for more than >160 generations. We constructed and phenotyped mitonuclear introgression lines, which allowed us to assess the independent effects of the evolutionary history of the nuclear and the mitochondrial genome. The nuclear genome was responsible for the largest share of divergence seen in ageing. However, the mitochondrial genome also had sizeable effects, which were sex‐specific and expressed primarily as epistatic interactions with the nuclear genome. The effects of mitonuclear disruption were largely consistent with mitonuclear coadaptation. Variation in ETC activity explained a large proportion of variance in ageing and life‐history traits and this multivariate relationship differed somewhat between the sexes. In conclusion, mitonuclear epistasis has played an important role in the laboratory evolution of ETC complex activity, ageing, and life histories and these are closely associated. The mitonuclear architecture of evolved differences in life‐history traits and mitochondrial bioenergetics was sex‐specific.     

The role of domestication and maternal effects on seed traits of crop–wild sunflower hybrids (Helianthus annuus)

Hybridisation between crops and their wild relatives may promote the evolution of weeds. Seed germination and dormancy are the earliest life‐history traits and are highly influenced by the maternal parent. However, the ecological role of the maternal effect on seed traits in the evolution of crop–wild hybrids has received little attention. In this study, we test the relative importance of maternal and hybridisation effects on seed traits of the first generation of crop–wild sunflower hybrids (Helianthus annuus). Seed germination was tested in two wild populations with contrasting dormancy, two cultivated materials and their reciprocal crosses at four different times after harvest and three different temperatures. Seed germination at each of the four times, after ripening response and secondary dormancy were recorded along with four morphological traits. Additionally, the pericarp anatomy was analysed with light and scanning electron microscopy. We observed strong maternal effects on all seed traits. Seed germination, morphology and pericarp anatomy differed largely between the crop and wild seeds and these traits in the crop–wild hybrids resembled their female parent. Slight but significant hybridisation effects were observed in germination, mainly in seeds produced on wild plants. Crop hybridisation changed seed germination, the after ripening response and secondary dormancy in the crop direction. Morphological and anatomical traits associated with domestication strongly correlated with the observed differences in seed germination and dormancy in crop–wild sunflower hybrids. The large maternal effects along with the evolutionary divergence in seed traits were responsible for the large phenotypic differences observed in crop–wild hybrids with the same genetic composition. Wild‐like seed traits of hybrids suggest that there are no barriers to crop gene introgression at the seed level whereas crop‐like seed traits could be strongly selected against, conditioning the selection of traits expressed later in the life cycle and in the next generations.     

Flower development schedule and AGAMOUS‐like gene expression patterns in two morphs of Nigella damascena (Ranunculaceae) differing in floral architecture

Love‐in‐a‐mist (Nigella damascena) is an annual species of Ranunculaceae native to the Mediterranean Basin, characterized by delicate flowers lying on long lacy bracts. Two floral morphs of N. damascena, designated [P] and [T], differ in the identity and number of perianth organs and in the position of the perianth–androecium boundary on the meristem. They both occur in the wild. Here we describe a precise comparative schedule of floral development in the two morphs. We divided the sequence of developmental events affecting the floral meristem into six stages and related them to the height of the elongating stem and to the time elapsed after the beginning of stem elongation. In addition, we characterized the expression pattern of C‐class genes in floral organs of both morphs in an attempt to better characterize the differences between the two floral groundplans. In the [T] morph an expansion of the expression domain of AGAMOUS (AG) paralogues outside the fertile organs was observed, correlating with the change in identity of the inner perianth organs. Expression of AG‐like genes in the sepal‐like organs suggests these are not identical to true sepals at the molecular level. The morpho‐temporal framework we have defined will allow us to compare various gene expression profiles at targeted developmental stages in both morphs, providing further insight into the molecular control of the floral dimorphism in N. damascena and into the processes underlying the transition from a differentiated (bipartite) to an undifferentiated (unipartite) perianth. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 178 , 608–619.     

Social Reversal of Sex‐Biased Aggression and Dominance in a Biparental Cichlid Fish (Julidochromis marlieri)

In biparental species, aggression, dominance, and parental care are typically sexually dimorphic. While behavioral dimorphism is often strongly linked to gonadal sex, the environment—either social or ecological—may also influence sex‐biased behavior. In the biparental cichlid fish Julidochromis marlieri, the typical social environment for breeding pairs consists of large females paired with smaller males. While both sexes are capable of providing territory defense and parental care, the larger female provides the majority of defense for the pair, while the smaller male remains in the nest guarding their offspring. We examine the contributions of sex and relative mate size to these sex‐biased behaviors in monogamous J. marlieri pairs. Both female‐larger and male‐larger pairs were formed in the laboratory and were observed for territorial aggression (against conspecifics and heterospecifics), dominance, and parental care. In female‐larger pairs, territorial aggression and intra‐pair dominance were female‐biased, while in male‐larger pairs this bias was reversed. For both pairing types, the presence of an intruder amplified sex differences in territorial aggression, with the larger fish always attacking with greater frequency than its mate. Though less robust, there was evidence for plasticity of sex‐bias for some egg care related behaviors in the inverse direction. Our study suggests that relative mate size strongly influences the sex bias of aggression and dominance in J. marlieri and that this aspect of the social environment can override the influence of gonadal sex on an individual's behavior. The remarkable plasticity of this species makes Julidochromis an exciting model that could be used to address the relationship between proximate and ultimate mechanisms of behavioral plasticity.     

Priority effects on the life‐history traits of two carrion blow fly (Diptera,Calliphoridae) species

1. Third instars of the invasive blow fly Chrysomya rufifacies are facultative predators on larvae of the native blow fly Cochliomyia macellaria. 2. The effects of priority arrival time on the survivorship and fitness of C. rufifacies and C. macellaria were investigated in laboratory experiments. 3. Cochliomyia macellaria colonising a resource within 1–2 days after C. rufifacies resulted in a 20–70% reduction in survivorship, pupal weight and fecundity compared with those colonising a resource more than 2 days before or after C. rufifacies. Inversely, C. rufifacies exhibited a 50% increase in survivorship and fecundity when closely (～2 days) associated temporally on the resource with C. macellaria and was negatively affected by disparate arrival. 4. These results demonstrate that arrival sequence significantly affects the fitness of both C. rufifacies and C. macellaria. Early colonisation may allow C. macellaria to persist in a community, while there are fitness benefits for C. rufifacies colonising after C. macellaria. 5. The 60% reduction in C. macellaria survivorship when in close temporal association with C. rufifacies may act as an agent of selection for C. macellaria to colonise a resource early and develop quickly to avoid predation on resources colonised by C. rufifacies. 6. Selection for such traits may explain how C. macellaria is able to persist despite intraguild predation by this invasive species. In contrast, the 50% increase in survivorship and fecundity exhibited by C. rufifacies when arriving after C. macellaria may select for C. rufifacies to delay colonisation.     

Precocious sexual dimorphism and the Lilliput effect in Neo‐Tethyan Ostracoda (Crustacea) through the Permian–Triassic boundary

The Elikah River section spanning the Lopingian (Late Permian) to the Griesbachian (Early Triassic) time interval in the Central Alborz Mountains (north Iran) was sampled for ostracod analysis. We report 79 species distributed among 38 genera. Four new species are described: Acratia? pervagata Forel sp. nov., Microcheilinella alborzella Forel sp. nov., Basslerella superarella Crasquin sp. nov. and Cavellina nesenensis Crasquin sp. nov. The ontogeny of 13 species is described and sexual dimorphism in the genus Microcheilinella is here undoubtedly recognized for the first time. Six species show precocious sexual dimorphism of their carapace as early as A‐5 juvenile. The Lilliput effect is for the first time recorded and quantified for two species. Rare long‐time span Palaeocopida species, known throughout the entire Permian, document relatively long‐term evolution, including the size and growth rate modifications associated with the earlier appearance of carapace sexual dimorphism through time. These patterns might be related to the Guadalupian–Lopingian events and/or to climatic modifications occurring during the Permian interval.     

Ecological patterns and genetic analysis of post‐dispersal seed predation in sunflower (Helianthus annuus) crop‐wild hybrids

Crop‐wild hybridization has been documented in many cultivated species, but the ecological and genetic factors that influence the likelihood or rate that cultivar alleles will introgress into wild populations are poorly understood. Seed predation is one factor that could mitigate the spread of otherwise advantageous cultivar alleles into the wild by reducing seedling recruitment of crop‐like individuals in hybrid populations. Seed predation has previously been linked to several seed characters that differ between cultivated and wild sunflower, such as seed size and oil content. In this study, seed morphological and nutritional characters were measured in a segregating population of sunflower crop‐wild hybrids and wild and cultivated lines. Seed predation rates among lines were then assessed in the field. The relationship between seed predation and seed characters was investigated and quantitative trait loci (QTL) were mapped for all traits. There was no effect of seed type (hybrid vs. parents) on seed predation, although a trend toward more early predation of wild seeds was observed. Within the hybrids, seed predators preferred seeds that contained more oil and energy but were lower in fibre. The relationship between seed predation and oil content was supported by co‐localized QTL for these traits on one linkage group. These results suggest that oil content may be a more important determinant of seed predation than seed size and provide molecular genetic evidence for this relationship. The cultivar allele was also found to increase predation at all QTL, indicating that post‐dispersal seed predation may mitigate the spread of cultivar alleles into wild populations.     

Comparison of seed and seedling functional traits in native Helianthus species and the crop H. annuus (sunflower)

• Seed functional traits of native Helianthus species contribute towards ecosystem services but limitations to their use in managed programmes exist. Many perennial Helianthus possess seed dormancy. The ability for germination to occur under different temperature and drought conditions, as well as the capacity of germinated seeds to convert into normal seedlings is rarely considered. Our aim was to identify and quantify these constraints through functional trait analyses.
• In five seed lots of native Helianthus (four perennial and one annual) and five genotypes of sunflower (H. annuus) for comparison, dormancy, thermal and hydro thresholds and times, morphology, mass, oil content and conversion into normal seedlings were quantified. The influence of the seed collection site environment on these traits was also explored.
• Seed dormancy of the perennial species was overcome by scarification followed by germination in 5 mm GA₃. Thermal and hydro‐time analyses revealed slower germination for the native seed lots (>1350 °Ch) in comparison to the sunflower genotypes (<829.9 °Ch). However, native seed lots had a higher capacity to convert into normal seedlings at high temperatures and low water potentials than sunflower genotypes. For the native seed lots, the average monthly temperature of the collection site was negatively correlated with thermal time.
• Variability in seed functional traits of native Helianthus and greater capacity for germinated seeds to convert into normal seedlings suggests they are better equipped to cope with high temperature and drought scenarios than sunflower. Effective dormancy alleviation is required to facilitate the use of native Helianthus species.

     

Differential self‐fertilization rates in response to variation in floral traits within inflorescences of Aquilegia buergeriana var. oxysepala (Ranunculaceae)

To assess variation in the proportion of self‐fertilized seeds among flowers within inflorescences and the relationship between floral traits and the rate of self‐fertilization, the proportion of self‐fertilized seeds among individual flowers was estimated using ten microsatellite markers in self‐compatible plants of Aquilegia buergeriana var. oxysepala. Within‐inflorescence variation in floral traits, such as the duration of the male and female phases, flower size, herkogamy and the number of pollen grains and ovules in two natural populations, were investigated. The first flower in an inflorescence produced more seeds and a higher proportion of self‐fertilized seeds than the second flower. The higher proportion of self‐fertilized seeds in the first flowers was accompanied by a higher number of pollen grains and ovules in the bud stage and the female phase. These results indicate that the high proportion of self‐fertilized seeds in the first flowers in an inflorescence may be due to the high number of remaining pollen grains in the female phase. This suggests that variation in floral traits within inflorescences affects seed quality and quantity among flowers within inflorescences.