Frugivorous birds mediate sex‐biased facilitation in a dioecious nurse plant

Abstract. Facilitation by dispersal occurs if the nurse plant acts as a focus which is actively selected by seed dispersers and enhances the fitness of the facilitated plant. Sex‐biased facilitation may be produced if seed dispersers tend to concentrate the seeds under female, fruit‐bearing plants of dioecious species more often than under conspecific males. Juniperus sabina is a dioecious shrub with a prostrate growth form from Mediterranean high mountains that modifies many microhabitat characteristics related to seedling establishment and survival. Soil water availability, maximum soil temperature in summer, organic matter and total nitrogen content, were different on open ground as compared with beneath J. sabina shrubs, irrespective of its sex. Other studied characteristics such as soil bulk density and soil compaction after rain did not differ between the microhabitats considered. Some species, such as Juniperus communis, Pinus nigra, Helleborus foetidus and Euphorbia nicaeensis, are spatially associated to J. sabina shrubs, strongly suggesting a facilitative role. The anemochorous P. nigra and myrme‐chorous H. foetidus and E. nicaeensis did not associate preferentially to any sex of J. sabina. Only J. communis, an endozoochorous species sharing the same bird dispersers as J. sabina, presented a female‐biased spatial association with the nurse plant. Seed dispersal mediated by birds attracted by the fruit‐rewarding females of J. sabina explains the sex‐biased spatial pattern of Juniperus communis.     

Pinus monophylla establishment in an expanding Pinus‐Juniperus woodland: Environmental conditions,facilitation and interacting factors

Abstract. The tree species comprising Pinus‐Juniperus woodlands are rapidly expanding into shrub‐grasslands throughout their range. Observational studies indicate that establishment is facilitated by nurse plants, but little information exists on the mechanisms involved. I examined both abiotic and biotic factors influencing Pinus monophylla establishment in Artemisia tridentata steppe with expanding populations of P. monophylla and Juniperus osteosperma. I determined soil water contents, temperatures, and nutrient characteristics for the primary establishment microhabitats, i.e. under Pinus, under Juniperus, under Artemisia, tree interspace and sage interspace, and evaluated the emergence and survival response of two seedling cohorts over a 3‐yr period for the different microhabitats. I also examined the effects of seed burial and predation on seedling establishment. Microhabitats under trees and shrubs had higher extractable P and K, higher organic matter, total nitrogen and cation exchange capacity than interspace microhabitats. Soil water contents (0–15 cm) were lower in interspaces than under shrubs or trees due to dry surface (0–5 cm) soils. Soil temperatures (at 1 and 15 cm) were lowest under trees, intermediate under shrubs, and highest in interspaces. Timing and rate of seedling emergence were temperature dependent with the order of emergence paralleling mean growing season temperatures: tree interspace = shrub interspace > under shrub > under Juniperus under Pinus. Seed burial was required for rooting and the highest emergence occurred from depths of 1 and 3 cm indicating that caching by birds and rodents is essential and that animals bury seeds at adequate if not optimal depths for emergence. Seedlings required microenvironmental modification for survival; all seedlings, including those that emerged from seeds and transplants, died within the first year in interspace microhabitats. Survival in under‐tree or under‐shrub microhabitats depended on soil water availability and corresponded closely to soil water contents over the 3‐yr study. Under‐shrub microhabitats had more favourable soil and micro‐environmental characteristics than under‐tree microhabitats and had the highest seedling life spans for the first‐year seedling cohort. Predation of Pinus seedlings by rodents was a significant cause of mortality with caged transplants exhibiting life spans that were 74% longer overall than uncaged transplants. Emergence and survival of P. monophylla within the expanding woodland were dependent upon a complex set of interacting factors including growing season conditions, microhabitat characteristics, and animal species.     

Genetic diversity,population structure and sex‐biased dispersal in three co‐evolving species

Genetic diversity and spatial structure of populations are important for antagonistic coevolution. We investigated genetic variation and population structure of three closely related European ant species: the social parasite Harpagoxenus sublaevis and its two host species Leptothorax acervorum and Leptothorax muscorum. We sampled populations in 12 countries and analysed eight microsatellite loci and an mtDNA sequence. We found high levels of genetic variation in all three species, only slightly less variation in the host L. muscorum. Using a newly introduced measure of differentiation (Jost’s D_est ), we detected strong population structuring in all species and less male‐biased dispersal than previously thought. We found no phylogeographic patterns that could give information on post‐glacial colonization routes – northern populations are as variable as more southern populations. We conclude that conditions for Thompson’s geographic mosaic of coevolution are ideal in this system: all three species show ample genetic variation and strong population structure.     

Fragmentation reduces regional‐scale spatial genetic structure in a wind‐pollinated tree because genetic barriers are removed

Gene flow strongly influences the regional genetic structuring of plant populations. Seed and pollen dispersal patterns can respond differently to the increased isolation resulting from habitat fragmentation, with unpredictable consequences for gene flow and population structuring. In a recently fragmented landscape we compared the pre‐ and post‐fragmentation genetic structure of populations of a tree species where pollen and seed dispersal respond differentially to forest fragmentation generated by flooding. Castanopsis sclerophylla is wind‐pollinated, with seeds that are dispersed by gravity and rodents. Using microsatellites, we found no significant difference in genetic diversity between pre‐ and post‐fragmentation cohorts. Significant genetic structure was observed in pre‐fragmentation cohorts, due to an unknown genetic barrier that had isolated one small population. Among post‐fragmentation cohorts this genetic barrier had disappeared and genetic structure was significantly weakened. The strengths of genetic structuring were at a similar level in both cohorts, suggesting that overall gene flow of C. sclerophylla has been unchanged by fragmentation at the regional scale. Fragmentation has blocked seed dispersal among habitats, but this appears to have been compensated for by enhanced pollen dispersal, as indicated by the disappearance of a genetic barrier, probably as a result of increased wind speeds and easier pollen movement over water. Extensive pollen flow can counteract some negative effects of fragmentation and assist the long‐term persistence of small remnant populations.     

A sex‐linked SCAR marker in Bryonia dioica (Cucurbitaceae), a dioecious species with XY sex‐determination and homomorphic sex chromosomes

Genetic crosses between the dioecious Bryonia dioica (Cucurbitaceae) and the monoecious B. alba in 1903 provided the first clear evidence for Mendelian inheritance of dioecy and made B. dioica the first organism for which XY sex‐determination was experimentally proven. Applying molecular tools to this system, we developed a sex‐linked sequence‐characterized amplified region (SCAR) marker for B. dioica and sequenced it for individuals representing the full geographic range of the species from Scotland to North Africa. For comparison, we also sequenced this marker for representatives of the dioecious B. cretica, B. multiflora and B. syriaca, and monoecious B. alba. In no case did any individual, male or female, yield more than two haplotypes. In northern Europe, we found strong linkage between our marker and sex, with all Y‐sequences being identical to each other. In southern Europe, however, the linkage between our marker and sex was weak, with recombination detected within both the X‐ and the Y‐homologues. Population genetic analyses suggest that the SCAR marker experienced different evolutionary pressures in northern and southern Europe. These findings fit with phylogenetic evidence that the XY system in Bryonia is labile and suggest that the genus may be a good system in which to study the early steps of sex chromosome evolution.     

You'd better walk alone: Changes in forest composition affect pollination efficiency and pre‐dispersal cone damage in Iberian Juniperus thurifera forests

• Changes in land‐use patterns are a major driver of global environmental change. Cessation of traditional land‐use practices has led to forest expansion and shifts in forest composition. Consequently, former monospecific forests maintained by traditional management are progressing towards mixed forests. However, knowledge is scarce on how the presence of other tree species will affect reproduction of formerly dominant species. We explored this question in the wind‐pollinated tree Juniperus thurifera. We hypothesised that the presence of heterospecific trees would have a negative effect on cone production and on the proportion of cones attacked by specialised predators.
• We assessed the relative importance of forest composition on cone production, seed development and pre‐dispersal cone damage on nine paired pure and mixed J. thurifera forests in three regions across the Iberian Peninsula. The effects of forest composition on crop size, cone and seed characteristics, as well as damage by pre‐dispersal arthropods were tested using mixed models.
• Cone production was lower and seed abortion higher in mixed forests, suggesting higher pollination failure. In contrast, cone damage by arthropods was higher in pure forests, supporting the hypothesis that presence of non‐host plants reduces damage rates. However, the response of each arthropod to forest composition was species‐specific and the relative rates of cone damage varied depending on individual tree crops.
• Larger crop sizes in pure forests compensated for the higher cone damage rates, leading to a higher net production of sound seeds compared to mixed forests. This study indicates that ongoing changes in forest composition after land abandonment may impact tree reproduction.

     

Population genetic connectivity of an endemic New Zealand passerine after large‐scale local extirpations: a model of re‐colonization potential

Little is known about how a 70% loss of native forests has affected the genetic connectivity of remnant bird populations in New Zealand. We use the common and widely distributed New Zealand Bellbird Anthornis melanura as an indicator species of population connectivity for well‐flighted birds. Using eight microsatellite loci, we identified five main genetic populations in the North Island, South Island, sub‐Antarctic Auckland Islands and two small remnant island populations adjacent to a large region of avian extirpations in northern North Island. Only one remnant island population, on a 30‐year‐old conservation reserve at Tiritiri Matangi, displayed a clear signature of recent genetic bottleneck. The 7% migration rate at Tiritiri Matangi indicates that bottlenecks can be maintained despite habitat rehabilitation, possibly through behavioural barriers to gene flow. Adjacent to the same extirpation zone, Bellbirds on the Poor Knights Islands were found to have low genetic diversity and low re‐colonization potential. Two gaps concordant with deforestation patterns separated the Kapiti Coast of southern North Island from populations to both the north and the south. In summary, we identified linked avian habitats, as well as isolated and inbred populations and suggest that Bellbirds are good re‐colonizers. We emphasize the importance of genetic studies that assess animal dispersal among newly rehabilitated habitat patches.     

How relatedness between mates influences reproductive success: An experimental analysis of self‐fertilization and biparental inbreeding in a marine bryozoan

Kin associations increase the potential for inbreeding. The potential for inbreeding does not, however, make inbreeding inevitable. Numerous factors influence whether inbreeding preference, avoidance, or tolerance evolves, and, in hermaphrodites where both self‐fertilization and biparental inbreeding are possible, it remains particularly difficult to predict how selection acts on the overall inbreeding strategy, and to distinguish the type of inbreeding when making inferences from genetic markers. Therefore, we undertook an empirical analysis on an understudied type of mating system (spermcast mating in the marine bryozoan, Bugula neritina) that provides numerous opportunities for inbreeding preference, avoidance, and tolerance. We created experimental crosses, containing three generations from two populations to estimate how parental reproductive success varies across parental relatedness, ranging from self, siblings, and nonsiblings from within the same population. We found that the production of viable selfed offspring was extremely rare (only one colony produced three selfed offspring) and biparental inbreeding more common. Paternity analysis using 16 microsatellite markers confirmed outcrossing. The production of juveniles was lower for sib mating compared with nonsib mating. We found little evidence for consistent inbreeding, in terms of nonrandom mating, in adult samples collected from three populations, using multiple population genetic inferences. Our results suggest several testable hypotheses that potentially explain the overall mating and dispersal strategy in this species, including early inbreeding depression, inbreeding avoidance through cryptic mate choice, and differential dispersal distances of sperm and larvae.     

Genetic evidence for male‐biased dispersal in the Qinghai toad‐headed agamid Phrynocephalus vlangalii and its potential link to individual social interactions

Sex‐biased dispersal has profound impacts on a species' biology and several factors have been attributed to its evolution, including mating system, inbreeding avoidance, and social complexity. Sex‐biased dispersal and its potential link to individual social interactions were examined in the Qinghai toad‐headed agamid (Phrynocephalus vlangalii). We first determined the pattern of sex‐biased dispersal using population genetic methods. A total of 345 specimens from 32 sites in the Qaidam Basin were collected and genotyped for nine microsatellite DNA loci. Both individual‐based assignment tests and allele frequency‐based analyses were conducted. Females revealed much more genetic structure than males and all results were consistent with male‐biased dispersal. First‐generation migrants were also identified by genetic data. We then examined eight social interaction‐related morphological traits and explored their potential link to sex‐biased dispersal. Female residents had larger heads and longer tails than female migrants. The well‐developed signal system among females, coupled with viviparity, might make remaining on natal sites beneficial, and hence promote female philopatry. Dominant females with larger heads were more likely to stay. Contrary to females, male migrants had larger heads and belly patches than residents, suggesting that dispersal might confer selective advantages for males. Such advantages may include opportunities for multiple mating and escaping from crowded sites. Large belly patches and several other morphological traits may assist their success in obtaining mates during dispersal. Furthermore, a relatively high relatedness (R = 0.06) among females suggested that this species might have rudimentary social structure. Case studies in “less” social species may provide important evidence for a better understanding of sex‐biased dispersal.     

The Pillars of Hercules as a bathymetric barrier to gene flow promoting isolation in a global deep‐sea shark (Centroscymnus coelolepis)

Knowledge of the mechanisms limiting connectivity and gene flow in deep‐sea ecosystems is scarce, especially for deep‐sea sharks. The Portuguese dogfish (Centroscymnus coelolepis) is a globally distributed and near threatened deep‐sea shark. C. coelolepis population structure was studied using 11 nuclear microsatellite markers and a 497‐bp fragment from the mtDNA control region. High levels of genetic homogeneity across the Atlantic (Φ_ST = ?0.0091, F_ST = 0.0024, P > 0.05) were found suggesting one large population unit at this basin. The low levels of genetic divergence between Atlantic and Australia (Φ_ST = 0.0744, P < 0.01; F_ST = 0.0015, P > 0.05) further suggested that this species may be able to maintain some degree of genetic connectivity even across ocean basins. In contrast, sharks from the Mediterranean Sea exhibited marked genetic differentiation from all other localities studied (Φ_ST = 0.3808, F_ST = 0.1149, P < 0.001). This finding suggests that the shallow depth of the Strait of Gibraltar acts as a barrier to dispersal and that isolation and genetic drift may have had an important role shaping the Mediterranean shark population over time. Analyses of life history traits allowed the direct comparison among regions providing a complete characterization of this shark's populations. Sharks from the Mediterranean had markedly smaller adult body size and size at maturity compared to Atlantic and Pacific individuals. Together, these results suggest the existence of an isolated and unique population of C. coelolepis inhabiting the Mediterranean that most likely became separated from the Atlantic in the late Pleistocene.     

Divergence and molecular variation in common whelk Buccinum undatum (Gastropoda: Buccinidae) in Iceland: a trans‐Atlantic comparison

The dispersal and history of species affects their genetic population structure at both small and large geographical scales. The common whelk, Buccinum undatum, is a widespread subtidal gastropod in the North Atlantic that has no planktonic larvae and has thus limited dispersal capacity. The snail, which has been harvested by humans for centuries, is highly variable in morphology. To evaluate the population structure in the rich fishing grounds in western Iceland and its divergence from samples across the Atlantic, genetic patterns based on sequence variation in two mitochondrial (mt)DNA genes (COI and 16S) and five microsatellites were studied and compared with variation in populations from both sides of the Atlantic. Significant differences in allele and haplotype frequencies were found among samples separated by short distances along the coast of Iceland. Partition of the variation showed larger variance among samples obtained from distant regions than from neighbouring sites and genetic distances were correlated with geographical distance among populations in Europe. Phylogeographic patterns in mtDNA reveal different monophyletic lineages on both sides of the Atlantic, which predate the onset of the Ice Age and which may constitute cryptic species. Similar micro‐ and macrogeographical patterns were observed for the mtDNA and microsatellite markers, despite high frequencies of null alleles. Bayesian skyline reconstructions of the demographic history and mismatch distributions suggest that, although sizes of some populations were unaffected by Ice Age glaciations, others show signs of expansion after the Last Glacial Maximum. These phylogeographical patterns are consistent with patterns expected for low dispersal species that have survived in allopatric glacial refugial populations on both sides of the Atlantic and in deep‐sea refugia within each continent. The observed genetic structure has implications for conservation and sustainable management of the harvested populations. © 2013 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 111 , 145–159.     

Patterns of co‐occurrences in a killifish metacommunity are more related with body size than with species identity

Body size may be more important than species identity in determining species interactions and community structure. However, co‐occurrence of organisms has commonly been analysed from a taxonomic perspective and the body size is rarely taken into account. On six sampling occasions, we analysed patterns of killifish co‐occurrences in nestedness (tendency for less rich communities to be subsamples of the richest), checkerboard structure (tendency for species segregation), and modularity (tendency for groups to co‐occur more frequently than random expectation) in a pond metacommunity located in Uruguay. We contrasted co‐occurrence patterns among species and body size‐classes (individuals from different species were combined into size categories). The analysis was performed at two spatial scales: ponds (communities) and sample units within ponds. Observed nestedness was frequently smaller than the null expectation, with significantly greater deviations for body size‐classes than for species, and for sample units than for communities. At the sample unit level, individuals tended to segregate (i.e. clump into a checkerboard pattern) to a larger extent by body size rather than by taxonomy. Modularity was rarely detected, but nevertheless indicated a level of taxonomic organization not evident in nestedness or checkerboard indices. Identification of the spatial scale and organization at which ecological forces determine community structure is a basic requirement for advancement of robust theory. In our study system, these ecological forces probably structured the community by body sizes of interacting organisms rather than by species identities.     

Variation in the population structure between a natural and a human‐modified forest for a pioneer tropical tree species not restricted to large gaps

The distribution of tree species in tropical forests is generally related to the occurrence of disturbances and shifts in the local environmental conditions such as light, temperature, and biotic factors. Thus, the distribution of pioneer tree species is expected to vary according to the gap characteristics and with human disturbances. We asked whether there was variation in the distribution of a pioneer species under different environmental conditions generated by natural disturbances, and between two forests with contrasting levels of human disturbance. To answer this question, we studied the distribution patterns and population persistence of the pioneer tree species Croton floribundus in the size and age gap range of a primary Brazilian forest. Additionally, we compared the plant density of two size‐classes between a primary and an early successional human‐disturbed forest. Croton floribundus was found to be widespread and equally distributed along the gap‐size gradient in the primary forest. Overall density did not vary with gap size or age (F‐ratio = 0.062, P = 0.941), and while juveniles were found to have a higher density in the early successional forest (P = 0.021), tree density was found to be similar between forests (P = 0.058). Our results indicate that the population structure of a pioneer tree species with long life span and a broad gap‐size niche preference varied between natural and human‐disturbed forests, but not with the level of natural disturbance. We believe this can be explained by the extreme environmental changes that occur after human disturbance. The ecological processes that affect the distribution of pioneer species in natural and human‐modified forests may be similar, but our results suggest they act differently under the contrasting environmental conditions generated by natural and human disturbances.     

Sex‐specific estimates of dispersal show female philopatry and male dispersal in a promiscuous amphibian,the alpine salamander (Salamandra atra)

Amphibians display wide variations in life‐history traits and life cycles that should prove useful to explore the evolution of sex‐biased dispersal, but quantitative data on sex‐specific dispersal patterns are scarce. Here, we focused on Salamandra atra, an endemic alpine species showing peculiar life‐history traits. Strictly terrestrial and viviparous, the species has a promiscuous mating system, and females reproduce only every 3 to 4 years. In the present study, we provide quantitative estimates of asymmetries in male vs. female dispersal using both field‐based (mark–recapture) and genetic approaches (detection of sex‐biased dispersal and estimates of migration rates based on the contrast in genetic structure across sexes and age classes). Our results revealed a high level of gene flow among populations, which stems exclusively from male dispersal. We hypothesize that philopatric females benefit from being familiar with their natal area for the acquisition and defence of an appropriate shelter, while male dispersal has been secondarily favoured by inbreeding avoidance. Together with other studies on amphibians, our results indicate that a species' mating system alone is a poor predictor of sex‐linked differences in dispersal, in particular for promiscuous species. Further studies should focus more directly on the proximate forces that favour or limit dispersal to refine our understanding of the evolution of sex‐biased dispersal in animals.     

spip 1.0: a program for simulating pedigrees and genetic data in age‐structured populations

We present the program spip for simulating multilocus genetic data on individuals in age‐structured populations. In addition to genetic data on sampled individuals, the pedigree connecting all individuals in the population is recorded. This allows investigation of the relationship between family structure and population parameters. We foresee that spip will be useful for evaluating multilocus estimators of pairwise relatedness and population structure, and for simulating the distribution of relatedness in populations with varying demographies. It also provides a method for simulating genetic drift in complex populations.