Stepping-stone Migration Research Articles

Bactrocera dorsalis in the Indian Ocean: A tale of two invasions.

An increasing number of invasive fruit fly pests are colonizing new grounds. With this study, we aimed to uncover the invasion pathways of the oriental fruit fly, Bactrocera dorsalis into the islands of the Indian Ocean. By using genome-wide SNP data and a multipronged approach consisting of PCA, ancestry analysis, phylogenetic inference, and kinship networks, we were able to resolve two independent invasion pathways. A western invasion pathway involved the stepping-stone migration of B.dorsalis from the east African coast into the Comoros, along Mayotte and into Madagascar with a decreasing genetic diversity. The Mascarene islands (Reunion and Mauritius), on the contrary, were colonized directly from Asia and formed a distinct cluster. The low nucleotide diversity suggests that only a few genotypes invaded the Mascarenes. The presence of many long runs of homozygosity (ROH) in the introduced populations is indicative of population bottlenecks, with evidence of a more severe bottleneck for populations along the western migration pathway than on the Mascarene islands. More strict phytosanitary regulations are recommended in order to prevent the further spread of B.dorsalis.

Holocene climate changes explain the spatial pattern in genetic diversity in populations of Cyperus papyrus from Southeast Africa wetlands.

Wetlands are one of the most threatened ecosystems in the world because more than 70% of the area worldwide has been lost since 1900. Wetland plant species rely greatly on water for seeds and propagules, which may lead to a downstream unidirectional dispersal and accumulation of genetic diversity downstream. However, several species show no support for unidirectional genetic diversity, revealing the complexity of population dynamics and gene flow in wetlands. Here, we used microsatellite loci to address how the past demographic dynamics shaped the contemporary spatial pattern in genetic diversity and population structure of Cyperus papyrus in wetlands of Southeast Africa. Using spatially explicit analysis and coalescent modelling, we found no support for unidirectional dispersal. Instead, we found higher genetic diversity in populations upstream than downstream in the river basin. We also found high admixture among populations, most likely due to connections between adjacent river basins during sporadic floods, and ongoing gene flow due to bird-mediated seed dispersal. Our results suggest stepping-stone migration due to strong isolation-by-distance, but not necessarily unidirectional. Moreover, the past demographic dynamics in the Holocene shaped the current pattern of genetic diversity and structure, leading to higher genetic diversity in populations upstream the Zambezi river basin. Our results also point to the very low genetic diversity of C. papyrus populations in Southeast Africa and the need for management and conservation strategies to guarantee the long-term persistence of the species in the region.

Barrier to Gene Flow of Grey Mangrove Avicennia marina Populations in the Malay Peninsula as Revealed From Nuclear Microsatellites and Chloroplast Haplotypes

Contemporary mangrove forest areas took shape historically and their genetic connectivity depends on sea-faring propagules, subsequent settlement, and persistence in suitable environments. Mangrove species world-wide may experience genetic breaks caused by major land barriers or opposing ocean currents influencing their population genetic structure. For Malay Peninsula, several aquatic species showed strong genetic differentiation between East and West coast regions due to the Sunda shelf flooding since the Last Glacial Maximum. In this study genetic diversity and structure of Avicennia marina populations in Malay Peninsula were assessed using nuclear microsatellite markers and chloroplast sequences. Even though all populations showed identical morphological features of A. marina, three evolutionary significant units were obtained with nuclear and cytoplasmic markers. Avicennia marina along a 586 km stretch of the West coast differed strongly from populations along an 80 km stretch of the East coast featuring chloroplast capture of Avicennia alba in an introgressive A. marina. Over and above this expected East-West division, an intra-regional subdivision was detected among A. marina populations in the narrowest region of the Strait of Malacca. The latter genetic break was supported by an amova, structure, and barrier analysis whereas RST > FST indicated an evolutionary signal of long-lasting divergence. Two different haplotypes along the Western coast showed phylogeographic relationship with either a northern or a putative southern lineage, thereby assuming two Avicennia sources facing each other during Holocene occupation with prolonged separation in the Strait of Malacca. Migrate-n model testing supported a northward unidirectional stepping-stone migration route, although with an unclear directionality at the genetic break position, most likely due to weak oceanic currents. Low levels of genetic diversity and southward connectivity was detected for East coast Avicennia populations. We compared the fine-scale spatial genetic structure (FSGS) of Avicennia populations along the exposed coast in the East vs. the sheltered coast in the West. A majority of transects from both coastlines revealed no within-site kinship-based FSGS, although the remoteness of the open sea is important for Avicennia patches to maintain a neighborhood. The results provide new insights for mangrove researchers and managers for future in-depth ecological-genetic-based species conservation efforts in Malay Peninsula.

The genetics of phenotypic plasticity.XII. Temporal and spatial heterogeneity

To understand empirical patterns of phenotypic plasticity, we need to explore the complexities of environmental heterogeneity and how it interacts with cue reliability. I consider both temporal and spatial variation separately and in combination, the timing of temporal variation relative to development, the timing of movement relative to selection, and two different patterns of movement: stepping-stone and island. Among-generation temporal heterogeneity favors plasticity, while within-generation heterogeneity can result in cue unreliability. In general, spatial variation more strongly favors plasticity than temporal variation, and island migration more strongly favors plasticity than stepping-stone migration. Negative correlations among environments between the time of development and selection can result in seemingly maladaptive reaction norms. The effects of higher dispersal rates depend on the life history stage when dispersal occurs and the pattern of environmental heterogeneity. Thus, patterns of environmental heterogeneity can be complex and can interact in unforeseen ways to affect cue reliability. Proper interpretation of patterns of trait plasticity requires consideration of the ecology and biology of the organism. More information on actual cue reliability and the ecological and developmental context of trait plasticity is needed.

Early Pliocene range expansion of a clade of subterranean Pyrenean beetles

Aim To investigate the possibility of range expansion and diversification within the subterranean environment in a genus of troglobiont beetles of the family Leiodidae (Troglocharinus), which have a disjunct distribution between the Pyrenees and the Catalonian coast. Location North-eastern Iberian Peninsula. Methods We sequenced 4 kb of five mitochondrial and two nuclear genes of 50 specimens of 12 of the 18 species of Troglocharinus, plus several outgroups. We reconstructed a phylogeny using Bayesian inference and maximum likelihood, estimated divergence times using Bayesian probabilities and an a priori evolutionary rate, compared the diversification of the main clades within the genus, and reconstructed their ancestral distribution using maximum likelihood. Results We found strong support for the monophyly of Troglocharinus and the clades in each of the geographical areas, which diverged in the early Pliocene. The coastal clade was further divided into geographically well-defined lineages, separated by Quaternary deposits. The origin of the coastal clade was a single colonization in the early Pliocene from the central Pyrenees. The diversification of the Pyrenean clade followed a constant rate, while the diversification rate of the coastal clade significantly decreased through the Plio-Pleistocene transition. Main conclusions Troglocharinus expanded its range from its ancestral area in the central Pyrenees to the coast of Catalonia and subsequently diversified, probably within the subterranean environment. Our favoured scenario is a stepping-stone migration, with possibly short-distance dispersals through the surface, along the eastern margin of the north-eastern Ebro basin. The range expansion took place in a narrow temporal window with favourable conditions between the early Pliocene and the onset of the Mediterranean climate by the mid-Pliocene. Surface dispersal was probably severely limited afterwards, as shown by the fragmentation of the coastal lineage.

Global genetic population structure in the commercially exploited deep-sea teleost orange roughy (Hoplostethus atlanticus) based on microsatellite DNA analyses

The widely distributed teleost orange roughy, Hoplostethus atlanticus, has been one of the main species targeted in deep-sea fisheries. While morphometric, parasite and otolith analyses have generally found differentiation among populations within ocean basins, genetic techniques have shown contradictory results at different geographical scales. Here, we used nine microsatellite DNA loci to study genetic diversity and differentiation in orange roughy at a global scale using samples from New Zealand, Australia, Namibia, Chile, and the Northeast Atlantic Ocean. Additionally, temporal genetic variation was assessed for eight sites in Northern New Zealand sampled in two different years. The expected heterozygosity was high in all the sites, suggesting high levels of genetic diversity in orange roughy. Overall, we detected low but significant differentiation at the global scale: across the Southern hemisphere and between the Southern hemisphere regions and the Northeast Atlantic Ocean. However, genetic homogeneity was found between New Zealand and Australia. The present data does not showed temporal variation in orange roughy from Northern New Zealand. A pattern of isolation by distance at the global scale suggests stepping-stone migration, which is likely the result of active adult dispersal. This study revealed levels of genetic differentiation at the global scale that were undetected with mitochondrial DNA sequences analyses.

The influence of habitats on female mobility in Central and Western Africa inferred from human mitochondrial variation

BackgroundWhen studying the genetic structure of human populations, the role of cultural factors may be difficult to ascertain due to a lack of formal models. Linguistic diversity is a typical example of such a situation. Patrilocality, on the other hand, can be integrated into a biological framework, allowing the formulation of explicit working hypotheses. The present study is based on the assumption that patrilocal traditions make the hypervariable region I of the mtDNA a valuable tool for the exploration of migratory dynamics, offering the opportunity to explore the relationships between genetic and linguistic diversity. We studied 85 Niger-Congo-speaking patrilocal populations that cover regions from Senegal to Central African Republic. A total of 4175 individuals were included in the study.ResultsBy combining a multivariate analysis aimed at investigating the population genetic structure, with a Bayesian approach used to test models and extent of migration, we were able to detect a stepping-stone migration model as the best descriptor of gene flow across the region, with the main discontinuities corresponding to forested areas.ConclusionsOur analyses highlight an aspect of the influence of habitat variation on human genetic diversity that has yet to be understood. Rather than depending simply on geographic linear distances, patterns of female genetic variation vary substantially between savannah and rainforest environments. Our findings may be explained by the effects of recent gene flow constrained by environmental factors, which superimposes on a background shaped by pre-agricultural peopling.

Influence of finite‐sites mutation, population subdivision and sampling schemes on patterns of nucleotide polymorphism for species with molecular hyperdiversity

Molecular hyperdiversity has been documented in viruses, prokaryotes and eukaryotes. Such organisms undermine the assumptions of the infinite-sites mutational model, because multiple mutational events at a site comprise a non-negligible portion of polymorphisms. Moreover, different sampling schemes of individuals from species with subdivided populations can profoundly influence resulting patterns and interpretations of molecular variation. Inspired by molecular hyperdiversity in the nematode Caenorhabditis sp. 5, which exhibits average pairwise differences among synonymous sites of >5% as well as modest population structure, we investigated via coalescent simulation the joint effects of a finite-sites mutation (FSM) process and population subdivision on the variant frequency spectrum. From many demes interconnected through a stepping-stone migration model, we constructed local samples from a single deme, pooled samples from several demes and scattered samples of a single individual from numerous demes. Compared with a single panmictic population at equilibrium, we find that high population mutation rates induce a deficit of rare variants (positive Tajima's D) under a FSM model. Population structure also induces such a skew for local samples when migration is high and for pooled samples when migration is low. Contrasts of sampling schemes for C. sp. 5 imply high mutational input coupled with high migration. We propose that joint analysis of local, pooled and scattered samples for species with subdivided populations provides a means of improving inference of demographic history, by virtue of the partially distinct patterns of polymorphism that manifest when sequences are analyzed according to differing sampling schemes.

WHEN GAPS REALLY ARE GAPS: STATISTICAL PHYLOGEOGRAPHY OF HYDROTHERMAL VENT INVERTEBRATES

The invertebrate animals endemic to deep-sea hydrothermal vents are distributed intermittently along relatively linear oceanic ridge axes. A one-dimensional stepping-stone model, therefore, provides a reasonable starting hypothesis of population structure for these species. Nevertheless, population genetic studies of many species from eastern Pacific vents did not detect the expected signatures of isolation-by-distance (IBD). Instead, distinct patterns of geographical subdivision have been attributed to the unique dispersal modes of individual species, topographical discontinuities of the ridge axes, nonequilibrium metapopulation scenarios and cryptic species. Here, we reexamined these inferences in light of expectations generated by computer simulations of a one-dimensional stepping-stone model. We evaluated whether the previously inferred subdivisions are statistically robust to an alternative explanation that continuous stepping-stone migration has occurred along the ridge axes but discontinuities in the sampling design (gaps) have generated the apparent disjunctions. We found that previous inferences about barriers to gene flow (vicariance) were supported in many cases, but that failures to detect evidence for IBD could be explained by low statistical power associated with the sampling effort. The simulation approaches presented here might be useful for testing the significance of inferred phylogeographic gaps in other species.

Contrasted patterns of genetic variation in the dogwhelk Nucella lapillus along two putative post-glacial expansion routes

During the last glacial maximum, the dogwhelk Nucella lapillus, like many other rocky shore species, was eradicated from the west and largely confined to southern refugia in the east Atlantic. Using microsatellite markers, we studied the geographical distribution of population genetic diversity of N. lapillus along 2 putative post-glacial expansion routes: northward along the east shores of Europe, and westward across the via Iceland to North America. The patterns of genetic diversity and genetic structure along these 2 routes indicate that the trans- Atlantic expansion involved a stepping-stone migration from Europe to Iceland to North America, with rare long-distance dispersal causing serial bottleneck effects. Along the east route, however, long-distance dispersal seems to have occurred more often. These observations, under- pinned by hydrography, suggest that rafting could be a major agent of dispersal for marine species lacking planktonic life stages.

Evolution of Cyrtandra (Gesneriaceae) in the Pacific Ocean: the origin of a supertramp clade

Cyrtandra comprises at least 600 species distributed throughout Malesia, where it is known for many local endemics and in Polynesia and Micronesia, where it is present on most island groups, and is among the most successfully dispersing genera of the Pacific. To ascertain the origin of the oceanic Pacific island species of Cyrtandra, we sequenced the internal transcribed spacers of nuclear ribosomal DNA of samples from throughout its geographical range. Because all oceanic Pacific island species form a well-supported clade, these species apparently result from a single initial colonization into the Pacific, possibly by a species from the eastern rim of SE Asia via a NW-to-SE stepping stone migration. Hawaiian species form a monophyletic group, probably as a result of a single colonization. The Pacific island clade of Cyrtandra dispersed across huge distances, in contrast to the apparent localization of the SE Asian clades. Although highly vagile, the Pacific clade is restricted to oceanic islands. Individual species are often endemic to a single island, characteristic of the "supertramp" life form sensu Diamond (1974, Science 184: 803-806). The evolution of fleshy fruit within Cyrtandra provided an adaptation for colonization throughout the oceanic Pacific via bird dispersal from a single common ancestor.

The role of immigrants in the assembly of the South American rainforest tree flora

The Amazon lowland rainforest flora is conventionally viewed as comprising lineages that evolved in biogeographic isolation after the split of west Gondwana (ca. 100 Myr ago). Recent molecular phylogenies, however, identify immigrant lineages that arrived in South America during its period of oceanic isolation (ca. 100-3 Myr ago). Long-distance sweepstakes dispersal across oceans played an important and possibly predominant role. Stepping-stone migration from Africa and North America through hypothesized Late Cretaceous and Tertiary island chains may have facilitated immigration. An analysis of inventory plot data suggests that immigrant lineages comprise ca. 20% of both the species and individuals of an Amazon tree community in Ecuador. This is more than an order of magnitude higher than previous estimates. We also present data on the community-level similarity between South American and palaeotropical rainforests, and suggest that most taxonomic similarity derives from trans-oceanic dispersal, rather than a shared Gondwanan history.

Detecting clinal and balanced selection using spatial autocorrelation analysis under kin‐structured migration

Recently spatial autocorrelation has been employed to infer microevolutionary processes from patterns of genetic variation. In theory, different processes should show characteristic signature correlograms; e.g., clinal selection should produce correlograms decreasing from positive to negative autocorrelation, whereas uniform balanced selection should lead to no spatial autocorrelation. The ability of a statistical method such as spatial autocorrelation analysis to distinguish between these selective regimes or even to detect departures from neutrality is dependent on the strength of the evolutionary force and the population structure. Weak selection or migration will not be apparent against the expected background of stochastic noise. Moreover, the population structure may generate sufficient stochastic variation such that even strong evolutionary forces may fail to be detected. This study uses computer simulation to examine the effects of kin-structured migration and three different selective regimes on the shape of spatial correlograms to assess the ability of this technique to detect different microevolutionary processes. Genetic variation among 8 loci is simulated in a linear set of 25 artificial populations. Kin-structured stepping-stone migration among adjacent populations is modeled; directional, balanced, and clinal selection, as well as neutral loci are considered. These experiments show that strong selection produces correlograms of the predicted shape. However, with an anthropologically reasonable population structure, considerable stochastic variation among correlograms for different alleles may still exist. This suggests the need for caution in inferring genetic process from spatial patterns.

EVOLUTION OF ALTRUISM IN KIN-STRUCTURED AND RANDOM SUBDIVIDED POPULATIONS.

A. population structure favorable to the evolution of an altruistic trait is studied by Monte Carlo simulation. The model is based on a small-scale nonindustrial human society but seems generalizable to other highly social mammals. Three hierarchical levels are recognized: 1) the ecologically isolated local group (hamlet) which may be composed of kin and/or unrelated individuals; 2) the deme (settlement) comprising several such groups which interbreed; and 3) the set of demes (metapopulation) among which gene flow occurs. The first two levels of the model are based on D. S. Wilson's structured deme concept; the third allows for gene flow among demes in the metapopulation and for the structured diffusion of alleles across a wider area than might be included within the scope of a single deme. The simulation models genetic drift by a process of hamlet formation which may be random, or variously kin-structured. Hamlets may then become extinct based on a probability function of their gene frequencies. Individual selection within settlements is modeled deterministically, and gene flow among settlements is modeled as two-dimensional steppingstone migration of random or kin-structured groups. Results of the simulations show that, with realistic values for group sizes, moderate extinction rate, and high rates of migration (m > 27%), disadvantageous alleles (s = 10% and 25%) may increase markedly due to differential hamlet extinction over the course of 50 generations. The greater the degree of kin-structuring of founder groups, the higher the variance among hamlets and the faster the rate of increase of the allele for altruism. Nonetheless, even in some randomly founded groups, a clear increase in the altruism gene frequency occurred. It is also notable that kin-structured group selection by hamlet extinction may be effective when the initial frequency of altruism genes is very low (average of one per deme) and among a relatively small number of demes (25). Thus the process of group extinction in a hierarchically structured population allows rapid increase of an allele for altruism under plausible demographic conditions.

Kin groups and trait groups: population structure and epidemic disease selection.

A Monte Carlo simulation based on the population structure of a small-scale human population, the Semai Senoi of Malaysia, has been developed to study the combined effects of group, kin, and individual selection. The population structure resembles D.S. Wilson's structured deme model in that local breeding populations (Semai settlements) are subdivided into trait groups (hamlets) that may be kin-structured and are not themselves demes. Additionally, settlement breeding populations are connected by two-dimensional stepping-stone migration approaching 30% per generation. Group and kin-structured group selection occur among hamlets the survivors of which then disperse to breed within the settlement population. Genetic drift is modeled by the process of hamlet formation; individual selection as a deterministic process, and stepping-stone migration as either random or kin-structured migrant groups. The mechanism for group selection is epidemics of infectious disease that can wipe out small hamlets particularly if most adults become sick and social life collapses. Genetic resistance to a disease is an individual attribute; however, hamlet groups with several resistant adults are less likely to disintegrate and experience high social mortality. A specific human gene, hemoglobin E, which confers resistance to malaria, is studied as an example of the process. The results of the simulations show that high genetic variance among hamlet groups may be generated by moderate degrees of kin-structuring. This strong microdifferentiation provides the potential for group selection. The effect of group selection in this case is rapid increase in gene frequencies among the total set of populations. In fact, group selection in concert with individual selection produced a faster rate of gene frequency increase among a set of 25 populations than the rate within a single unstructured population subject to deterministic individual selection. Such rapid evolution with plausible rates of extinction, individual selection, and migration and a population structure realistic in its general form, has implications for specific human polymorphisms such as hemoglobin variants and for the more general problem of the tempo of evolution as well.

Protection of Recessive and Dominant Traits in a Subdivided Population with General Migration Structure.

The problem of migration-selection interaction in a subdivided population affecting a recessive allele is studied. Explicit conditions for protection of a recessive allele are determined, accessible for any migration structure. More specifically, consider allele a recessive to allele A distributed over N demes endowed with fitness parameters wi, 1, 1 for genotypes aa, Aa, and AA operating in deme i, respectively. For an arbitrary migration structure between demes summarized by the backward migration matrix, M = |mij|Ni,j=1 (mij = the proportion per generation of the population in deme i whose parents came from deme j), let $$\underline{\xi}$$ = (ξ1,..., ξN) be the unique left eigenvector of M corresponding to eigenvalue 1, whose sum is normalized to unity. The exact necessary and sufficient condition for protection of the recessive allele, a, is that the "weighted average" of the aa-genotype fitness values, namely ∑Ni=1 ξiwi, exceed unity. The result applies whether soft or hard selection is assumed. It is further established that, with a dominant or recessive trait, fixation of alleles a and A cannot coexist as stable alternatives. Interpretations and further applications of the conditions are given for some special migration patterns, including the stepping-stone migration mode and the generalized Island model gene flow.