Gene dispersal inference across forest patches in an endangered medicinal tree: comparison of model‐based approaches

Propagule dispersal in plants is a fundamental mechanism for colonizing new sites and adapting to changing climates, as well as for maintaining genetic diversity. Contrasting past and current gene dispersal can provide useful insights to gauge the extent of recent human disturbances and guide management strategies. However, research on gene dispersal of plants is not yet exhaustive because evolutionary or environmental impacts are often species‐specific and most existing studies have focused on analysis of dispersal at a single site, which may not be helpful for landscape‐level inferences and management interventions. In the present study, we assessed whether current gene or propagule dispersal would be more restricted than past gene dispersal at multiple patches of the endangered medicinal tree, Prunus africana. We employed eight highly polymorphic microsatellite markers in conjunction with isolation‐by‐distance, spatial genetic structure (SGS), and parentage assignment models to estimate gene dispersal distance in a spatial extent of approximately 400 km². There was no significant difference between gene dispersal distances across the different models (Friedman chi‐squared = 7.286, d.f. = 5, P = 0.2002). Estimates of current gene dispersal distance were comparable to dispersal in the last few generations. However, gene dispersal distance was much shorter in smaller than bigger forest patches. Further, significant (P < 0.05) SGS was detected in most forest patches, with the extent of SGS among adults being stronger in the smaller than bigger patches. These results suggest the need for practicing enrichment plantings in most forest patches, particularly in the smaller ones, to assist gene exchange among individuals and patches. © 2015 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 887–904.     

Estimating dispersal distributions at multiple scales: within‐colony and among‐colony dispersal rates,distances and directions in European Shags Phalacrocorax aristotelis

Knowledge of the rate, distance and direction of dispersal within and among breeding areas is required to understand and predict demographic and genetic connectivity and resulting population and evolutionary dynamics. However dispersal rates, and the full distributions of dispersal distances and directions, are rarely comprehensively estimated across all spatial scales relevant to wild populations. We used re‐sightings of European Shags Phalacrocorax aristotelis colour‐ringed as chicks on the Isle of May (IoM), UK, to quantify rates, distances and directions of dispersal from natal to subsequent breeding sites both within IoM (within‐colony dispersal) and across 27 other breeding colonies covering 1045 km of coastline (among‐colony dispersal). Additionally, we used non‐breeding season surveys covering 895 km of coastline to estimate breeding season detection probability and hence potential bias in estimated dispersal parameters. Within IoM, 99.6% of individuals dispersed between their natal and observed breeding nest‐site. The distribution of within‐colony dispersal distances was right‐skewed; mean distance was shorter than expected given random settlement within IoM, yet some individuals dispersed long distances within the colony. The distribution of within‐colony dispersal directions was non‐uniform but did not differ from expectation given the spatial arrangement of nest‐sites. However, 10% of all 460 colour‐ringed adults that were located breeding had dispersed to a different colony. The maximum observed dispersal distance (170 km) was much smaller than the maximum distance surveyed (690 km). The distribution of among‐colony dispersal distances was again right‐skewed. Among‐colony dispersal was directional, and differed from random expectation and from the distribution of within‐colony dispersal directions. Non‐breeding season surveys suggested that the probability of detecting a colour‐ringed adult at its breeding location was high in the northeastern UK (98%). Estimated dispersal rates and distributions were therefore robust to incomplete detection. Overall, these data demonstrate skewed and directionally divergent dispersal distributions across small (within‐colony) and large (among‐colony) scales, indicating that dispersal could create genetic and demographic connectivity within the study area.     

Plant dispersal strategies and the colonization of Araucaria forest patches in a grassland‐forest mosaic

Questions: In a natural grassland‐forest mosaic: What is the influence of phylogeny and diaspore traits related to disperser attraction (DAT) on (1) seed size/number trade‐off (SSNT) in woody species colonizing forest patches; (2) on the frequency of the species? 3. What is the influence of forest patch area on mean seed size and number. 4. Do phylogeny and DAT expressed at the species level affect this relationship? Location: Campos grassland and Araucaria forest in São Francisco de Paula, RS, Brazil, at ca. 29°28’ S; 50° 13’ W. Methods: Forest patches of different sizes in a grassland site recovering for ten years since human disturbances were surveyed by the relative abundance of vertebrate‐dispersed woody saplings. We described colonizer species according to taxonomic phylogenetic relationships and diaspore type, size and color. We analyzed with a variation partitioning method their influence on SSNT and on species frequency in the patches. At the community level we regressed mean seed size and number on forest patch area and evaluated how these relationships were affected by phylogeny and DAT at the species level. Results: 1. Phylogeny and DAT mostly explained seed size and seed number per diaspore variation. 2. By controlling phylogeny and DAT influence the frequency of species in forest patches was positively associated with their seed number in the diaspores, and negatively associated with their seed size. 3. Mean seed size and seed number at the community level were positively associated with patch area. 4. When phylogeny and DAT influences on seed size were removed this relationship was stronger for seed size and weaker for seed number. Conclusions: 1. Energy allocation to dispersal in detriment of offspring survival increased the successful establishment of colonizer species in forest patches, despite phylogenetic relationships and DAT variation in their diaspores. 2. Although patch area exerted a selective pressure on seed size, habitat preferences of dispersers may also influence patch colonization.     

Role of breeding and natal movements in lifetime dispersal of a forest‐dwelling rodent

The lifetime movements of an individual determine the gene flow and invasion potential of the species. However, sex dependence of dispersal and selective pressures driving dispersal have gained much more attention than dispersal at different life and age stages. Natal dispersal is more common than dispersal between breeding attempts, but breeding dispersal may be promoted by resource availability and competition. Here, we utilize mark–recapture data on the nest‐box population of Siberian flying squirrels to analyze lifetime dispersal patterns. Natal dispersal means the distance between the natal nest and the nest used the following year, whereas breeding movements refer to the nest site changes between breeding attempts. The movement distances observed here were comparable to distances reported earlier from radio‐telemetry studies. Breeding movements did not contribute to lifetime dispersal distance and were not related to variation in food abundance or habitat patch size. Breeding movements of males were negatively, albeit not strongly, related to male population size. In females, breeding movement activity was low and was not related to previous breeding success or to competition between females for territories. Natal philopatry was linked to apparent death of a mother; that is, we did not find evidence for mothers bequeathing territories for offspring, like observed in some other rodent species. Our results give an example of a species in which breeding movements are not driven by environmental variability or nest site quality. Different evolutionary forces often operate in natal and breeding movements, and our study supports the view that juveniles are responsible for redistributing individuals within and between populations. This emphasizes the importance of knowledge on natal dispersal, if we want to understand consequences of movement ecology of the species at the population level.     

Genetic diversity within and between remnant populations of the endangered calcareous grassland plant <Emphasis Type="Italic">Globularia bisnagarica</Emphasis> L.

Changes in agricultural production methods over the last century have caused a massive reduction and fragmentation of the area of European semi-natural grasslands. It remains unclear whether small and isolated grassland fragments can support viable plant populations in a sustainable way. In our study area in southern Belgium, the extent of calcareous grasslands was reduced from c. 650 ha in 1775 to less than 30 ha in 2004. We used AFLP markers to quantify the effects of present and historical grassland fragmentation on the genetic structure of 27 populations of the rare perennial plant species Globularia bisnagarica. Given the mixed breeding system of the species and the relatively small area of the studied system, the populations were characterized by high genetic differentiation (F _st range: 0.42–0.48; Φ_st=0.53). A Mantel test revealed significant isolation by distance of the populations. Average within population genetic diversity, measured as expected heterozygosity or gene diversity, was low (H _j =0.081) and was negatively related to population isolation. This suggests more gene flow into less isolated populations. Population size and local habitat characteristics did not significantly influence population genetic diversity. Both, high selfing rates in G. bisnagarica and a population genetic response to habitat fragmentation may explain our findings. Finally, a clear geographical clustering was observed, with cluster membership partially explainable by historical grassland connectivity. If populations indeed started to differentiate after fragmentation, this process was not (yet) strong enough to erase the genetic similarity between fragments that historically belonged to the same large grassland fragment.     

Spore sensitivity to sunlight and freezing can restrict dispersal in wood‐decay fungi

Assessment of the costs and benefits of dispersal is central to understanding species'' life-history strategies as well as explaining and predicting spatial population dynamics in the changing world. While mortality during active movement has received much attention, few have studied the costs of passive movement such as the airborne transport of fungal spores. Here, we examine the potential of extreme environmental conditions to cause dispersal mortality in wood-decay fungi. These fungi play a key role as decomposers and habitat creators in forest ecosystems and the populations of many species have declined due to habitat loss and fragmentation. We measured the effect of simulated solar radiation (including ultraviolet A and B) and freezing at −25°C on the spore germinability of 17 species. Both treatments but especially sunlight markedly reduced spore germinability in most species, and species with thin-walled spores were particularly light sensitive. Extrapolating the species'' laboratory responses to natural irradiance conditions, we predict that sunlight is a relevant source of dispersal mortality at least at larger spatial scales. In addition, we found a positive effect of spore size on spore germinability, suggesting a trade-off between dispersal distance and establishment. We conclude that freezing and particularly sunlight can be important sources of dispersal mortality in wood-decay fungi which can make it difficult for some species to colonize isolated habitat patches and habitat edges.     

Contrasting demographic and genetic estimates of dispersal in the endangered Coahuilan box turtle: a contemporary approach to conservation

The evolutionary viability of an endangered species depends upon gene flow among subpopulations and the degree of habitat patch connectivity. Contrasting population connectivity over ecological and evolutionary timescales may provide novel insight into what maintains genetic diversity within threatened species. We employed this integrative approach to evaluating dispersal in the critically endangered Coahuilan box turtle (Terrapene coahuila) that inhabits isolated wetlands in the desert‐spring ecosystem of Cuatro Ciénegas, Mexico. Recent wetland habitat loss has altered the spatial distribution and connectivity of habitat patches; and we therefore predicted that T. coahuila would exhibit limited movement relative to estimates of historic gene flow. To evaluate contemporary dispersal patterns, we employed mark–recapture techniques at both local (wetland complex) and regional (intercomplex) spatial scales. Gene flow estimates were obtained by surveying genetic variation at nine microsatellite loci in seven subpopulations located across the species’ geographical range. The mark–recapture results at the local spatial scale reveal frequent movement among wetlands that was unaffected by interwetland distance. At the regional spatial scale, dispersal events were relatively less frequent between wetland complexes. The complementary analysis of population genetic substructure indicates strong historic gene flow (global F_ST = 0.01). However, a relationship of genetic isolation by distance across the geographical range suggests that dispersal limitation exists at the regional scale. Our approach of contrasting direct and indirect estimates of dispersal at multiple spatial scales in T. coahuila conveys a sustainable evolutionary trajectory of the species pending preservation of threatened wetland habitats and a range‐wide network of corridors.     

Mind the gap: genetic distance increases with habitat gap size in Florida scrub jays

Habitat gap size has been negatively linked to movement probability in several species occupying fragmented landscapes. How these effects on movement behaviour in turn affect the genetic structure of fragmented populations at local scales is less well known. We tested, and confirmed, the hypothesis that genetic differentiation among adjacent populations of Florida scrub jays--an endangered bird species with poor dispersal abilities and a high degree of habitat specialization--increases with the width of habitat gaps separating them. This relationship was not an artefact of simple isolation-by-distance, as genetic distance was not correlated with the Euclidean distance between geographical centroids of the adjacent populations. Our results suggest that gap size affects movement behaviour even at remarkably local spatial scales, producing direct consequences on the genetic structure of fragmented populations. This finding shows that conserving genetic continuity for specialist species within fragmented habitat requires maintenance or restoration of preserve networks in which habitat gaps do not exceed a species-specific threshold distance.     

World phylogeography and male‐mediated gene flow in the sandbar shark,Carcharhinus plumbeus

The sandbar shark, Carcharhinus plumbeus, is a large, cosmopolitan, coastal species. Females are thought to show philopatry to nursery grounds while males potentially migrate long distances, creating an opportunity for male‐mediated gene flow that may lead to discordance in patterns revealed by mitochondrial DNA (mtDNA) and nuclear markers. While this dynamic has been investigated in elasmobranchs over small spatial scales, it has not been examined at a global level. We examined patterns of historical phylogeography and contemporary gene flow by genotyping 329 individuals from nine locations throughout the species’ range at eight nuclear microsatellite markers and sequencing the complete mtDNA control region. Pairwise comparisons often resulted in fixation indices and divergence estimates of greater magnitude using mtDNA sequence data than microsatellite data. In addition, multiple methods of estimation suggested fewer populations based on microsatellite loci than on mtDNA sequence data. Coalescent analyses suggest divergence and restricted migration among Hawaii, Taiwan, eastern and western Australia using mtDNA sequence data and no divergence and high migration rates, between Taiwan and both Australian sites using microsatellite data. Evidence of secondary contact was detected between several localities and appears to be discreet in time rather than continuous. Collectively, these data suggest complex spatial/temporal relationships between shark populations that may feature pulses of female dispersal and more continuous male‐mediated gene flow.     

Selection and sex‐biased dispersal in a coastal shark: the influence of philopatry on adaptive variation

Sex‐biased dispersal is expected to homogenize nuclear genetic variation relative to variation in genetic material inherited through the philopatric sex. When site fidelity occurs across a heterogeneous environment, local selective regimes may alter this pattern. We assessed spatial patterns of variation in nuclear‐encoded, single nucleotide polymorphisms (SNPs) and sequences of the mitochondrial control region in bonnethead sharks (Sphyrna tiburo), a species thought to exhibit female philopatry, collected from summer habitats used for gestation. Geographic patterns of mtDNA haplotypes and putatively neutral SNPs confirmed female philopatry and male‐mediated gene flow along the northeastern coast of the Gulf of Mexico. A total of 30 outlier SNP loci were identified; alleles at over half of these loci exhibited signatures of latitude‐associated selection. Our results indicate that in species with sex‐biased dispersal, philopatry can facilitate sorting of locally adaptive variation, with the dispersing sex facilitating movement of potentially adaptive variation among locations and environments.     

Genetic assignment of recruits reveals short‐ and long‐distance larval dispersal in Pocillopora damicornis on the Great Barrier Reef

Understanding connectivity of coral populations among and within reefs over ecologically significant timescales is essential for developing evidence‐based management strategies, including the design of marineprotected areas. Here, we present the first assessment of contemporary connectivity among populations of two Molecular Operational Taxonomic Units (MOTUs) of the brooding coral Pocillopora damicornis. We used individual‐based genetic assignment methods to identify the proportions of philopatric and migrant larval recruits, settling over 12 months at sites around Lizard Island (northern Great Barrier Reef [GBR]) and over 24 months at sites around the Palms Islands (central GBR). Overall, we found spatially and temporally variable rates of self‐recruitment and dispersal, demonstrating the importance of variation in local physical characteristics in driving dispersal processes. Recruitment patterns and inferred dispersal distances differed between the two P. damicornis MOTUs, with type α recruits exhibiting predominantly philopatric recruitment, while the majority of type β recruits were either migrants from identified putative source populations or assumed migrants based on genetic exclusion from all known populations. While P. damicornis invests much energy into brooding clonal larvae, we found that only 15% and 7% of type α and type β recruits, respectively, were clones of sampled adult colonies or other recruits, challenging the hypothesis that reproduction is predominantly asexual in this species on the GBR. We explain high rates of self‐recruitment and low rates of clonality in these MOTUs by suggesting that locally retained larvae originate predominantly from spawned gametes, while brooded larvae are mainly vagabonds.     

Similarity in temporal variation in sex‐biased dispersal over short and long distances in the dark‐eyed junco,Junco hyemalis

Patterns of sex‐biased dispersal (SBD) are typically consistent within taxa, for example female‐biased in birds and male‐biased in mammals, leading to theories about the evolutionary pressures that lead to SBD. However, generalizations about the evolution of sex biases tend to overlook that dispersal is mediated by ecological factors that vary over time. We examined potential temporal variation in between‐ and within‐population dispersal over an 11‐year period in a bird, the dark‐eyed junco (Junco hyemalis). We measured between‐population dispersal patterns using genetic assignment indices and found yearly variation in which sex was more likely to have immigrated. When we measured within‐population spatial genetic structure and mark–recapture dispersal distances, we typically found yearly SBD patterns that mirrored between‐population dispersal, indicating common eco‐evolutionary causes despite expected differences due to the scale of dispersal. However, in years without detectable between‐population sex biases, we found genetic similarity between nearby males within our population. This suggests that, in certain circumstances, ecological pressures may act on within‐population dispersal without affecting dispersal between populations. Alternatively, current analytical tools may be better able to detect within‐population SBD. Future work will investigate potential causes of the observed temporal variation in dispersal patterns and whether they have greater effects on within‐population dispersal.     

Male‐biased dispersal and the potential impact of human‐induced habitat modifications on the Neotropical bat Trachops cirrhosus

Gene flow, maintained through natal dispersal and subsequent mating events, is one of the most important processes in both ecology and population genetics. Among mammalian populations, gene flow is strongly affected by a variety of factors, including the species’ ability to disperse, and the composition of the environment which can limit dispersal. Information on dispersal patterns is thus crucial both for conservation management and for understanding the social system of a species. We used 16 polymorphic nuclear microsatellite loci in addition to mitochondrial DNA sequences (1.61 kbp) to analyse the population structure and the sex‐specific pattern of natal dispersal in the frog‐eating fringe‐lipped bat, Trachops cirrhosus, in Central Panama. Our study revealed that—unlike most of the few other investigated Neotropical bats—gene flow in this species is mostly male‐mediated. Nevertheless, distinct genetic clusters occur in both sexes. In particular, the presence of genetic differentiation in the dataset only consisting of the dispersing sex (males) indicates that gene flow is impeded within our study area. Our data are in line with the Panama Canal in connection with the widening of the Río Chagres during the canal construction acting as a recent barrier to gene flow. The sensitivity of T. cirrhosus to human‐induced habitat modifications is further indicated by an extremely low capture success in highly fragmented areas. Taken together, our genetic and capture data provide evidence for this species to be classified as less mobile and thus vulnerable to habitat change, information that is important for conservation management.     

Sex‐biased dispersal and high levels of gene flow among local populations in the argentine boa constrictor,Boa constrictor occidentalis

Abstract The knowledge of dispersal is essential to understand the ecology of any species, since population dynamics, spatial distribution and genetic structure are closely tied to patterns of movement. In this paper we estimate dispersal patterns in natural populations of the endangered snake Boa constrictor occidentalis (Serpentes, Boidae), using allozymes as genetic markers. Blood samples were obtained from a total of 120 adult individuals of nine localities from two areas, Sobremonte and Pocho, in Argentina. Only four out of a total of 24 loci were polymorphic: 6‐Pgdh‐1, Cat‐1, Ldh and Hp. The values of expected and observed mean heterozygosities, the percentage of polymorphic loci and mean number of alleles per locus for each population confirm the low levels of genetic variability in this snake. F_ST and N_em mean values were 0.0089 and 46.1 for Sobremonte and 0.0379 and 7.46 for Pocho, indicating important levels of gene flow. A comparison of F_ST between genders in both areas suggests a male‐biased dispersal, which could be explained by the characteristics of the mating system: males carry out an active mate search of receptive females, and philopatry could be selected in females due to the benefits of the familiarity with the natal area in the use of local resources.     

The utility of contemporary and historical estimates of dispersal in determining response to habitat fragmentation in a tropical forest-dependent bird community

It is often assumed that species which exhibit a greater propensity for dispersal are less susceptible to the impacts of habitat fragmentation; however, a growing body of literature suggests that such generalizations should be carefully evaluated as not all species appear to be equally sensitive to fragmentation. In this issue of Molecular Ecology, Callens et al. (2011) take an innovative approach to compare contemporary estimates of dispersal from an extensive mark-recapture and patch occupancy data set with historical estimates derived from multilocus population genetic models for seven sympatric forest-dependent species in the Taita Hills, Africa. As has been observed for forest-dependent species from the Amazon, populations of sedentary species were more strongly differentiated and clustered when compared to those of more dispersive taxa. The most intriguing result recovered though, was that the five species with similar historical estimates of gene flow (dispersal) differed substantially in their contemporary dispersal rates, suggesting that for some species the propensity for dispersal has decreased over time. As a consequence, the authors suggest that post-fragmentation estimates of dispersal on their own may not be the best predictors of how habitat fragmentation could affect forest-dependent animal communities.This work significantly advances our understanding of the dynamics of habitat fragmentation and makes a strong case for the need to integrate data on historical processes with contemporary data.     

Long‐term ‘islands’ in the landscape: low gene flow,effective population size and genetic divergence in the shrub Hakea oldfieldii (Proteaceae)

The genetic structure of disjunct populations is determined by founding genetic properties, demographic processes, gene flow, drift and local selection. We aim to identify the genetic consequences of natural population disjunction at regional and local scales in Hakea oldfieldii using nuclear and plastid markers to investigate long‐term effective population sizes and gene flow, and patterns of diversity and divergence, among populations. Regional divergence was significant as shown by a consistent pattern in principal coordinates, neighbor‐joining and Bayesian analyses, but divergence at the local level was also significant with localized distribution of plastid haplotypes and populations clustering separately in Bayesian analyses. Historical, recent and first‐generation gene flow was low, suggesting that recent habitat fragmentation has not reduced gene migration significantly. Genetic bottlenecks were detected in three populations. Long‐term effective population size was significantly correlated with the number of alleles/locus and observed heterozygosity, but not with census population size, suggesting that the loss of diversity is associated with long‐term changes rather than recent fragmentation. Inbreeding coefficients were significant in only three populations, suggesting that the loss of diversity is linked to drift and bottlenecks associated with demographic processes (local extinction by fires) rather than inbreeding. Historical disjunction as a result of specific ecological requirements, contraction of habitats following drying during the Pleistocene, low gene flow and changes in population size are likely to have been important forces driving divergence through isolation by distance and drift. © 2015 The Linnean Society of London, Botanical Journal of the Linnean Society, 2015, 179 , 319–334.