High Potential For Gene Flow Research Articles

Demographic history has shaped the strongly differentiated corkwing wrasse populations in Northern Europe.

Understanding the biological processes involved in genetic differentiation and divergence between populations within species is a pivotal aim in evolutionary biology. One particular phenomenon that requires clarification is the maintenance of genetic barriers despite the high potential for gene flow in the marine environment. Such patterns have been attributed to limited dispersal or local adaptation, and to a lesser extent to the demographic history of the species. The corkwing wrasse (Symphodus melops) is an example of a marine fish species where regions of particular strong divergence are observed. One such genetic break occurred at a surprisingly small spatial scale (FST ~0.1), over a short coastline (<60km) in the North Sea-Skagerrak transition area in southwestern Norway. Here, we investigate the observed divergence and purported reproductive isolation using genome resequencing. Our results suggest that historical events during the post-glacial recolonization route can explain the present population structure of the corkwing wrasse in the northeast Atlantic. While the divergence across the break is strong, we detected ongoing gene flow between populations over the break suggesting recent contact or negative selection against hybrids. Moreover, we found few outlier loci and no clear genomic regions potentially being under selection. We concluded that neutral processes and random genetic drift e.g., due to founder events during colonization have shaped the population structure in this species in Northern Europe. Our findings underline the need to take into account the demographic process in studies of divergence processes.

RADseq and mate choice assays reveal unidirectional gene flow among three lamprey ecotypes despite weak assortative mating: Insights into the formation and stability of multiple ecotypes in sympatry.

Adaptive divergence with gene flow often results in complex patterns of variation within taxa exhibiting substantial ecological differences among populations. One example where this may have occurred is the parallel evolution of freshwater-resident nonparasitic lampreys from anadromous-parasitic ancestors. Previous studies have focused on transitions between these two phenotypic extremes, but here, we considered more complex evolutionary scenarios where an intermediate freshwater form that remains parasitic is found sympatrically with the other two ecotypes. Using population genomic analysis (restriction-associated DNA sequencing), we found that a freshwater-parasitic ecotype was highly distinct from an anadromous-parasitic form (Qlake-P =96.8%, Fst =0.154), but that a freshwater-nonparasitic form was almost completely admixed in Loch Lomond, Scotland. Demographic reconstructions indicated that both freshwater populations likely derived from a common freshwater ancestor. However, while the nonparasitic ecotype has experienced high levels of introgression from the anadromous-parasitic ecotype (Qanad-P =37.7%), there is no evidence of introgression into the freshwater-parasitic ecotype. Paradoxically, mate choice experiments predicted high potential for gene flow: Males from all ecotypes were stimulated to spawn with freshwater-parasitic females, which released gametes in response to all ecotypes. Differentially fixed single nucleotide polymorphisms identified genes associated with growth and development, which could possibly influence the timing of metamorphosis, resulting in significant ecological differences between forms. This suggests that multiple lamprey ecotypes can persist in sympatry following shifts in adaptive peaks, due to environmental change during their repeated colonization of post-glacial regions, followed by periods of extensive gene flow among such diverging populations.

Linking genetic and ecological differentiation in an ungulate with a circumpolar distribution

Genetic differentiation among populations may arise from the disruption of gene flow due to local adaptation to distinct environments and/or neutral accumulation of mutations and genetic drift resulted from geographical isolation. Quantifying the role of these processes in determining the genetic structure of natural populations remains challenging. Here, we analyze the relative contribution of isolation‐by‐resistance (IBR), isolation‐by‐environment (IBE), genetic drift and historical isolation in allopatry during Pleistocene glacial cycles on shaping patterns of genetic differentiation in caribou/reindeer populations Rangifer tarandus across the entire distribution range of the species. Our study integrates analyses at range‐wide and regional scales to partial out the effects of historical and contemporary isolation mechanisms. At the circumpolar scale, our results indicate that genetic differentiation is predominantly explained by IBR and historical isolation. At a regional scale, we found that IBR, IBE and population size significantly explained the spatial distribution of genetic variation among populations belonging to the Euro‐Beringian lineage within North America. In contrast, genetic differentiation among populations within the North American lineage was predominantly explained by IBR and population size, but not IBE. We also found discrepancies between genetic and ecotype designation across the Holarctic species distribution range. Overall, these results indicate that multiple isolating mechanisms have played roles in shaping the spatial distribution of genetic variation across the distribution range of a large mammal with high potential for gene flow. Considering multiple spatial scales and simultaneously testing a comprehensive suite of potential isolating mechanisms, our study contributes to understand the ecological and evolutionary processes underlying organism–landscape interactions.

Population Structure and Adaptive Divergence in a High Gene Flow Marine Fish: The Small Yellow Croaker (Larimichthys polyactis).

The spatial distribution of genetic diversity has been long considered as a key component of policy development for management and conservation of marine fishes. However, unraveling the population genetic structure of migratory fish species is challenging due to high potential for gene flow. Despite the shallow population differentiation revealed by putatively neutral loci, the higher genetic differentiation with panels of putatively adaptive loci could provide greater resolution for stock identification. Here, patterns of population differentiation of small yellow croaker (Larimichthys polyactis) were investigated by genotyping 15 highly polymorphic microsatellites in 337 individuals of 15 geographic populations collected from both spawning and overwintering grounds. Outlier analyses indicated that the locus Lpol03 might be under directional selection, which showed a strong homology with Grid2 gene encoding the glutamate receptor δ2 protein (GluRδ2). Based on Lpol03, two distinct clusters were identified by both STRUCTURE and PCoA analyses, suggesting that there were two overwintering aggregations of L. polyactis. A novel migration pattern was suggested for L. polyactis, which was inconsistent with results of previous studies based on historical fishing yield statistics. These results provided new perspectives on the population genetic structure and migratory routes of L. polyactis, which could have significant implications for sustainable management and utilization of this important fishery resource.

Regional environmental pressure influences population differentiation in turbot (Scophthalmus maximus)

Unravelling the factors shaping the genetic structure of mobile marine species is challenging due to the high potential for gene flow. However, genetic inference can be greatly enhanced by increasing the genomic, geographical or environmental resolution of population genetic studies. Here, we investigated the population structure of turbot (Scophthalmus maximus) by screening 17 random and gene-linked markers in 999 individuals at 290 geographical locations throughout the northeast Atlantic Ocean. A seascape genetics approach with the inclusion of high-resolution oceanographical data was used to quantify the association of genetic variation with spatial, temporal and environmental parameters. Neutral loci identified three subgroups: an Atlantic group, a Baltic Sea group and one on the Irish Shelf. The inclusion of loci putatively under selection suggested an additional break in the North Sea, subdividing southern from northern Atlantic individuals. Environmental and spatial seascape variables correlated marginally with neutral genetic variation, but explained significant proportions (respectively, 8.7% and 10.3%) of adaptive genetic variation. Environmental variables associated with outlier allele frequencies included salinity, temperature, bottom shear stress, dissolved oxygen concentration and depth of the pycnocline. Furthermore, levels of explained adaptive genetic variation differed markedly between basins (3% vs. 12% in the North and Baltic Sea, respectively). We suggest that stable environmental selection pressure contributes to relatively strong local adaptation in the Baltic Sea. Our seascape genetic approach using a large number of sampling locations and associated oceanographical data proved useful for the identification of population units as the basis of management decisions.

Evolutionary History of Lake Tanganyika's Predatory Deepwater Cichlids.

Hybridization among littoral cichlid species in Lake Tanganyika was inferred in several molecular phylogenetic studies. The phenomenon is generally attributed to the lake level-induced shoreline and habitat changes. These allow for allopatric divergence of geographically fragmented populations alternating with locally restricted secondary contact and introgression between incompletely isolated taxa. In contrast, the deepwater habitat is characterized by weak geographic structure and a high potential for gene flow, which may explain the lower species richness of deepwater than littoral lineages. For the same reason, divergent deepwater lineages should have evolved strong intrinsic reproductive isolation already in the incipient stages of diversification, and, consequently, hybridization among established lineages should have been less frequent than in littoral lineages. We test this hypothesis in the endemic Lake Tanganyika deepwater cichlid tribe Bathybatini by comparing phylogenetic trees of Hemibates and Bathybates species obtained with nuclear multilocus AFLP data with a phylogeny based on mitochondrial sequences. Consistent with our hypothesis, largely congruent tree topologies and negative tests for introgression provided no evidence for introgressive hybridization between the deepwater taxa. Together, the nuclear and mitochondrial data established a well-supported phylogeny and suggested ecological segregation during speciation.

Influence of environmental heterogeneity on genetic diversity and structure in an endemic southern Californian oak

Understanding how specific environmental factors shape gene flow while disentangling their importance relative to the effects of geographical isolation is a major question in evolutionary biology and a specific goal of landscape genetics. Here, we combine information from nuclear microsatellite markers and ecological niche modelling to study the association between climate and spatial genetic structure and variability in Engelmann oak (Quercus engelmannii), a wind-pollinated species with high potential for gene flow. We first test whether genetic diversity is associated with climatic niche suitability and stability since the Last Glacial Maximum (LGM). Second, we use causal modelling to analyse the potential influence of climatic factors (current and LGM niche suitability) and altitude in the observed patterns of genetic structure. We found that genetic diversity is negatively associated with local climatic stability since the LGM, which may be due to higher immigration rates in unstable patches during favourable climatic periods and/or temporally varying selection. Analyses of spatial genetic structure revealed the presence of three main genetic clusters, a pattern that is mainly driven by two highly differentiated populations located in the northern edge of the species distribution range. After controlling for geographic distance, causal modelling analyses showed that genetic relatedness decreases with the environmental divergence among sampling sites estimated as altitude and current and LGM niche suitability. Natural selection against nonlocal genotypes and/or asynchrony in reproductive phenology may explain this pattern. Overall, this study suggests that local environmental conditions can shape patterns of genetic structure and variability even in species with high potential for gene flow and relatively small distribution ranges.

Local adaptation in populations of a Brachionus group plicatilis cryptic species inhabiting three deep crater lakes in Central Mexico

Summary1. Salinity is a strong selective force for many aquatic organisms, affecting both ecological and evolutionary processes. Most of our knowledge on the effects of salinity on rotifers in the Brachionus plicatilis species complex is based mainly on populations from waterbodies that experience broad environmental changes both seasonally and annually. We tested the hypothesis that, despite the supposedly high potential for gene flow among rotifers inhabiting neighbouring environments, constant salinity has promoted local adaptation, genetic population divergence and even cryptic speciation in B. plicatilis complex populations from three deep maar lakes of distinct salinities [1.1, 6.5 and 9.0 g L−1 total dissolved solids (TDS)] in Central Mexico.2. To look for local adaptation, we performed common garden experiments to test the effect of different salinities on population density and intrinsic growth rate (r). Then, we evaluated the genetic divergence by sequencing the cytochrome c oxidase subunit I (COI) gene and performed reproductive trials to assess the potential gene flow among the three populations and with other closely related B. plicatilis complex species.3. We confirmed that the rotifer populations have phenotypic plasticity in tolerance of salinity, but only rotifers from the least saline lake are adapted to low salinity. Among the populations, sequence divergence at COI was very low (just a single haplotype was found), suggesting a persistent founder effect from a relatively recent single colonisation event and a subsequent dispersal from one lake to the others, and a very restricted immigration rate. In the phylogenetic analysis, rotifers from this area of Mexico clustered in the same clade with the middle‐sized species Brachionus ibericus and B. sp. ‘Almenara’. Mexican rotifers showed successful recognition, copulation and formation of hybrids among them, but interpopulation breeding with the Spanish B. ibericus and B. sp. ‘Almenara’ was unsuccessful.4. We conclude that the B. plicatilis complex populations from these three lakes belong to a new biological species not yet described (presently named B. sp. ‘Mexico’). To our knowledge, this is the first report of local adaptation of a natural B. plicatilis complex population living in freshwater conditions (1.1 g L−1 TDS).

Population differentiation and restricted gene flow in Spanish crossbills: not isolation‐by‐distance but isolation‐by‐ecology

Divergent selection stemming from environmental variation may induce local adaptation and ecological speciation whereas gene flow might have a homogenizing effect. Gene flow among populations using different environments can be reduced by geographical distance (isolation-by-distance) or by divergent selection stemming from resource use (isolation-by-ecology). We tested for and encountered phenotypic and genetic divergence among Spanish crossbills utilizing different species of co-occurring pine trees as their food resource. Morphological, vocal and mtDNA divergence were not correlated with geographical distance, but they were correlated with differences in resource use. Resource diversity has now been found to repeatedly predict crossbill diversity. However, when resource use is not 100% differentiated, additional characters (morphological, vocal, genetic) must be used to uncover and validate hidden population structure. In general, this confirms that ecology drives adaptive divergence and limits neutral gene flow as the first steps towards ecological speciation, unprevented by a high potential for gene flow.

RESISTANCE TO BIOTIC STRESS IN FRUIT TREES

Resistance to pests and diseases is a highly desirable objective in fruit breeding but is a long-term endeavor. It requires appropriate tests for early screening and an analysis of host-parasite interactions for durability of resistance. Host resistance is considered durable when it remains effective for a long period despite an intensive exposure to the parasite. Durability has to be the key-point of any fruit breeding programme for resistance. Non-durable resistance is usually associated with a hypersensitive reaction (HR) and major gene resistance which often occur in multiple allelic series and/or complex loci. HR resistance or race-specific resistance is often rendered ineffective because the pathogen population shifts genetically to avoid the resistance gene. Resistance of a more durable nature against fungi and bacteria is often polygenic and based upon the additive or interaction effects of a few to several genes not promoting a hypersensitive reaction. The more complex the genetics of the resistance, the more difficult it is for the pathogen to evolve to a form that can overcome the resistance. Polygenic resistance is usually associated with a quantitative expression that is characterized by a continuous variation between susceptibility and resistance. To approach the number of genes involved in polygenic resistance (QTL) and the relative effect of each of these genes, they have to be mapped on the genome. Marker-assisted selection (MAS) gives the possibility to recombine QTL for resistance; major genes could be associated with QTL. The combining of resistance genes is desired to: acquire a higher level of resistance against a particular pathotype, obtain resistance against a broader range of pathotypes, and combine different mechanisms of resistance. The current situation of fruit crops - monocultivar orchards established for several years - enhances the selection pressure on the pathogen population and results in population shifts which could be dramatic. Guidelines have to be proposed to predict the evolutionary potential of pathogen populations based on analysis of their genetic structure; the most important parameters to consider are reproductive/mating systems and gene/genotype flow. Pathogens that have the greatest risk of breaking down resistance genes are those that possess a mixed reproduction system, with one sexual cycle per growing season and asexual reproduction during the epidemic phase, and a high potential for gene flow. Several examples of different strategies used by fruit breeders will be reported mainly on Coffea (coffee rust), Musa (black leaf streak disease), Prunus (root knot nematodes) and Malus (scab, mildew, fire blight). Fruit breeders can use the lessons learned from deploying resistance genes in annual crops and selecting resistance in forest trees and apply these to their strategies for fruit tree improvement

The population genetics of plant pathogens and breeding strategies for durable resistance

The durability of disease resistance is affected by the evolutionary potential of the pathogen population. Pathogens with a high evolutionary potential are more likely to overcome genetic resistance than pathogens with a low evolutionary potential. We will propose a set of guidelines to predict the evolutionary potential of pathogen populations based on analysis of their genetic structure. Under our model of pathogen evolution, the two most important parameters to consider are reproduction/mating system and gene/genotype flow. Pathogens that pose the greatest risk of breaking down resistance genes are those that possess a mixed reproduction system, with at least one sexual cycle per growing season and asexual reproduction during the epidemic phase, and a high potential for gene flow. The lowest risk pathogens are those with strict asexual reproduction and low potential for gene flow. We will present examples of high- and low-risk pathogens. Knowledge of the population genetic structure of the pathogen may offer insight into the best breeding strategy for durable resistance. We will present broad guidelines suggesting a rational method for breeding durable resistance according to the population genetics of the pathogen.

Evidence for broadscale introgressive hybridization between two redfish (genus Sebastes) in the North-west Atlantic: a rare marine example.

The evolutionary importance of introgressive hybridization has long been recognized by plant evolutionists, and there is now a growing recognition for its potential role in animals as well. Detailed empirical investigations of this evolutionary process, however, are still lacking in many animal groups, particularly in the marine environment. Using integrated microsatellite DNA data (eight loci analysed over 803 individuals representing 17 sampling locations) and multivariate statistical procedures (principal component, factorial correspondence and admixture proportion analyses), we: (i) provide a detailed dissection of the dynamics of introgressive hybridization between Sebastes fasciatus and S. mentella, two economically important redfishes from the North-west Atlantic; and (ii) infer the factors potentially involved in the maintenance of the hybrid zone observed in the gulf of St. Lawrence and south of Newfoundland. This study provided one of the rare examples of extensive introgressive hybridization in the ocean, and highlighted the predominant role of this process in shaping the extent of genetic diversity, interspecific differences and population structuring among redfishes from the North-west Atlantic. The extensive (average rate of introgression = 15%) but geographically circumscribed and asymmetrical pattern of introgressive hybridization, the sympatric persistence of two reproductively isolated introgressed groups, the differential patterns of linkage disequilibrium among samples, and the maintenance of genetic integrity of both species outside the defined zone of introgression despite high potential for gene flow, all implicated selection in promoting and maintaining the observed pattern of introgression.

SPECIATION AND POPULATION GENETIC STRUCTURE IN TROPICAL PACIFIC SEA URCHINS

Unlike populations of many terrestrial species, marine populations often are not separated by obvious, permanent barriers to gene flow. When species have high dispersal potential and few barriers to gene flow, allopatric divergence is slow. Nevertheless, many marine species are of recent origin, even in taxa with high dispersal potential. To understand the relationship between genetic structure and recent species formation in high dispersal taxa, we examined population genetic structure among four species of sea urchins in the tropical Indo-West Pacific that have speciated within the past one to three million years. Despite high potential for gene flow, mtDNA sequence variation among 200 individuals of four species in the urchin genus Echinometra shows a signal of strong geographic effects. These effects include (1) substantial population heterogeneity; (2) lower genetic variation in peripheral populations; and (3) isolation by distance. These geographic patterns are especially strong across scales of 5000-10,000 km, and are weaker over scales of 2500-5000 km. As a result, strong geographic patterns would not have been readily visible except over the wide expanse of the tropical Pacific. Surface currents in the Pacific do not explain patterns of gene flow any better than do patterns of simple spatial proximity. Finally, populations of each species tend to group into large mtDNA regions with similar mtDNA haplotypes, but these regional boundaries are not concordant in different species. These results show that all four species have accumulated mtDNA differences over similar spatial and temporal scales but that the precise geographic pattern of genetic differentiation varies for each species. These geographic patterns appear much less deterministic than in other well-known coastal marine systems and may be driven by chance and historical accident.

Genetic Variation among South American Populations of Tetraploid Chenopodium sect. Chenopodium subsect. Cellulata

Electrophoretic analysis of South American Chenopodium (sect. Che- nopodium subsect. Cellulata, 2n = 4x = 36) reveals multi-locus isozyme systems for leucine aminopeptidase (LAP) and phosphoglucoisomerase (PGI) that appear to be the result of tetraploid gene duplication. The bi-locus LAP system is monomorphic for active alleles with putative null alleles at each locus that are not present in pop- ulations at the northern range extreme. The null allele at Lap-i appears to be sporadically distributed in the highlands of Peru, Bolivia, and Argentina, whereas the null variant at Lap-2 shows a clinal increase from north to south with fixation in the Argentine lowlands. All material (62 population samples from Chile, Argen- tina, Bolivia, and Peru, and 206 exemplar samples from Ecuador, Peru, and Bolivia) is monomorphic at Pg'-I and essentially monomorphic at the other two PGI loci, with the exception of low elevation populations of Argentina, which show five active variants and one null. Aside from clinal trends at two loci, the observed pattern of genetic variation is not consistent with extreme discontinuities in selective regime, habitat, and distribution. It is proposed that an archaic genotype has been conserved in the Andean area of chenopod cultivation through interpopulation gene flow me- diated by weed-crop genetic interaction and human dispersal. A relatively high level of inter-population reproductive isolation in lowland Argentina has possibly allowed differentiation of PGI alleles and silencing of one LAP locus through fixation of null alleles. Populations from lowland Argentina include individuals showing electro- phoretic diploidization in both isozyme systems, thus producing the typical pheno- type of diploid Chenopodium. The percentage of heterozygous plants per population and level of detected out-crossing indicate a high potential for gene flow within populations of lowland Argentina, although genetic interaction with sympatric C. album was not detected.

GEOGRAPHIC VARIATION IN THE MILKFISH CHANOS CHANOS. I. BIOCHEMICAL EVIDENCE.

Since the first use of protein gel electrophoresis for the assessment of genic variation in natural populations (Lewontin and Hubby, 1966), a large number of plants and animals across many phylogenetic lines has been surveyed for electrophoretic variation. Results of these surveys and synopses of the related evolutionary hypotheses have been summarized in Lewontin (1974), Ayala (1976), and Nevo (1978). In reviewing these reports, it is apparent that one group of organisms has been generally overlooked: the marine fishes. For instance, many workers have examined the population structure of freshwater fishes (Avise and Selander, 1972; Avise and Smith, 1974; Echelle et al., 1975; Allendorf et al., 1976; Vrijenhoek et al., 1977; and others), yet there are virtually no data available for widely distributed marine fishes. In comparable studies of marine fishes, the work has dealt with diadromous fishes (Koehn and Williams, 1978; Utter et al., 1980), estuarine fishes (Johnson, 1975), or fishes from restricted geographic areas (Gorman et al., 1976; Gorman and Kim, 1977; Ward and Beardmore, 1977). In only one report were genetic differences assessed for a marine fish found in separate localities across the tropics, but this study remains unpublished (Soule, reference in Ehrlich, 1975). It is generally assumed that because of a planktonic larval stage, marine fish have a high potential for gene flow and hence may show little interlocality differentiation, but this topic remains unexplored. It would be interesting, therefore, to assess patterns of geographic differentiation of fish populations within and among archipelagos across an ocean basin. It has long been realized that small and/ or isolated populations may undergo considerable genetic changes. Semi-isolated populations of cavefish Astyanax mexicanus had reduced levels of electrophoretic variation relative to conspecific surface populations (Avise and Selander, 1972), and stream populations of Etheostoma radiosum, separated in different drainages of the same tributary, exhibited high levels of population differentiation (Echelle et al., 1975). In a marine habitat the epitome of isolation of an ichthyofauna is the Hawaiian inshore fish community. Randall (1976) estimates the level of endemism for the inshore fishes is 29%-the highest value for any oceanic island. Yet, there have been no electrophoretic estimates of the degree of isolation of the fishes in Hawaii. Thus, using electrophoretic data, the following questions were examined for the milkfish Chanos chanos: 1) What is the level of genic variation in this species and how does it change over large geographic distances? 2) What is the genetic population structure for a marine fish, such as Chanos, that has a planktonic larval stage? 3) What factors affect the observed pattern of geographic variation and how does the level of geographic differentiation compare to that of other species-terrestrial and marine? 4) How genetically isolated is the Hawaiian population of milkfish relative to other milkfish populations? Life history of milkfish. -Milkfish, Chanos chanos (Forskal), are tropical marine fish distributed throughout the Pacific 1 Hawaii Institute of Marine Biology Contribution No. 586.