Parapatric Populations Research Articles

NATURAL SELECTION IN POPULATIONS SUBJECT TO A MIGRATION LOAD

Migration tends to oppose the effects of divergent natural selection among populations. Numerous theoretical and empirical studies have demonstrated that this migration-selection balance constrains genetic divergence among populations. In contrast, relatively few studies have examined immigration's effects on fitness and natural selection within recipient populations. By constraining local adaptation, migration can lead to reduced fitness, known as a "migration load," which in turn causes persistent natural selection. We develop a simple two-island model of migration-selection balance that, although very general, also reflects the natural history of Timema cristinae walking-stick insects that inhabit two host plant species that favor different cryptic color patterns. We derive theoretical predictions about how migration rates affect the level of maladaptation within populations (measured as the frequency of less-cryptic color-pattern morphs), which in turn determines the selection differential (the within-generation morph frequency change). Using data on color morph frequencies from 25 natural populations, we confirm previous results showing that maladaptation is higher in populations receiving more immigrants. We then present novel evidence that this increased maladaptation leads to larger selection differentials, consistent with our model. Our results provide comparative evidence that immigration elevates the variance in fitness, which in turn leads to larger selection differentials, consistent with Fisher's Theorem of Natural Selection. However, we also find evidence that recurrent adult migration between parapatric populations may tend to obscure the effects of selection.

The evolution of host preference in allopatric vs. parapatric populations of Timema cristinae walking-sticks

Divergent habitat preferences can contribute to speciation, as has been observed for host-plant preferences in phytophagous insects. Geographic variation in host preference can provide insight into the causes of preference evolution. For example, selection against maladaptive host-switching occurs only when multiple hosts are available in the local environment and can result in greater divergence in regions with multiple vs. a single host. Conversely, costs of finding a suitable host can select for preference even in populations using a single host. Some populations of Timema cristinae occur in regions with only one host-plant species present (in allopatry, surrounded by unsuitable hosts) whereas others occur in regions with two host-plant species adjacent to one another (in parapatry). Here, we use host choice and reciprocal-rearing experiments to document genetic divergence in host preference among 33 populations of T. cristinae. Populations feeding on Ceanothus exhibited a stronger preference for Ceanothus than did populations feeding on Adenostoma. Both allopatric and parapatric pairs of populations using the different hosts exhibited divergent host preferences, but the degree of divergence tended to be greater between allopatric pairs. Thus, gene flow between parapatric populations apparently constrains divergence. Host preferences led to levels of premating isolation between populations using alternate hosts that were comparable in magnitude to previously documented premating isolation caused by natural and sexual selection against migrants between hosts. Our findings demonstrate how gene flow and different forms of selection interact to determine the magnitude of reproductive isolation observed in nature.

Evidence for a Müllerian mimetic radiation in Asian pitvipers

Müllerian mimicry, in which toxic species gain mutual protection from shared warning signals, is poorly understood in vertebrates, reflecting a paucity of examples. Indirect evidence for mimicry is found if monophyletic species or clades show parallel geographic variation in warning patterns. Here, we evaluate a hypothesis of Müllerian mimicry for the pitvipers in Southeast Asia using a phylogeny derived from DNA sequences from four combined mitochondrial regions. Mantel matrix correlation tests show that conspicuous red colour pattern elements are significantly associated with sympatric and parapatric populations in four genera. To our knowledge, this represents the first evidence of a Müllerian mimetic radiation in vipers. The putative mimetic patterns are rarely found in females. This appears paradoxical in light of the Müllerian prediction of monomorphism, but may be explained by divergent selection pressures on the sexes, which have different behaviours. We suggest that biased predation on active males causes selection for protective warning coloration, whereas crypsis is favoured in relatively sedentary females.

Genital lock-and-key system and premating isolation by mate preference in carabid beetles (Carabus subgenus Ohomopterus)

The shapes and lengths of copulatory pieces and vaginal appendices of the carabid beetle subgenus Ohomopterus (genus Carabus) vary among species. In Japan, the species in the group with a medium body size (C. yaconinus, C. iwawakianus, C. maiyasanus, C. uenoi, C. arrowianus, C. esakii, and C. insulicola) are usually allopatric or parapatric, except at Mt Kongosan, where C. uenoi, C. iwawakianus, and C. yaconinus are sympatrically distributed. The degree of premating isolation by mate preference was high between sympatric populations, irrespective of the genetic distance between them. However, premating isolation was absent between parapatric populations. The degree of premating isolation for allopatric populations spanned a wide range of isolation values. Thus, mate discrimination by males seems to have evolved mostly between sympatric pairs. These results suggest two hypotheses. First, premating isolation has evolved through reinforcement or through reproductive character displacement after sympatric contact. Second, premating isolation has evolved in allopatry, and as a result of premating isolation, the species can coexist in sympatry. We also examined the degree of mechanical isolation between C. uenoi and C. iwawakianus (a sympatric pair), which have a very large difference in the length of the copulatory piece. The insertion success was low and only one female produced viable offspring among 15 crosses; however, death in females due to copulation was rare. For sympatric matings between C. uenoi and C. iwawakianus, a large difference in the genital size might reduce the gene flow with small mating costs. Gene flow that was significantly reduced by genital difference might cause either the evolution of premating isolation through reinforcement/reproductive character displacement or through the maintenance of a high degree of premating isolation following sympatric contact. © 2006 The Linnean Society of London, Biological Journal of the Linnean Society, 2006, 87, 145–154.

Habitat structure and the dispersal of male and female bottlenose dolphins (Tursiops truncatus)

Bottlenose dolphins (Tursiops truncatus) are widely distributed and a high degree of morphometric and genetic differentiation has been found among both allopatric and parapatric populations. We analysed 145 samples along a contiguous distributional range from the Black Sea to the eastern North Atlantic for mitochondrial and nuclear genetic diversity, and found population structure with boundaries that coincided with transitions between habitat regions. These regions can be characterized by ocean floor topography, and oceanographic features such as surface salinity, productivity and temperature. At the extremes of this range there was evidence for the directional emigration of females. Bi-parentally inherited markers did not show this directional bias in migration, suggesting a different dispersal strategy for males and females at range margins. However, comparative assessment based on mitochondrial DNA and nuclear markers indicated that neither sex showed a strong bias for greater dispersal on average. These data imply a mechanism for the evolutionary structuring of populations based on local habitat dependence for both males and females.

A secondary hybrid zone between diploid Dactylorhiza incarnata ssp. cruenta and allotetraploid D. lapponica (Orchidaceae)

Secondary hybrid zones are not uncommon in Dactylorhiza, but knowledge of ecological and evolutionary consequences of hybridization are scarce. Here, we assess interploidal gene flow and introgression in a hybrid zone between diploid Dactylorhiza incarnata ssp. cruenta (2n = 2x = 40) and its putative allotetraploid derivative D. lapponica (2n = 4x = 80). Photometric quantification of DNA content and morphology confirmed that triploids are abundant in sympatric populations in our study area. Allozyme segregation patterns in D. lapponica supported an allopolyploid origin, although unbalanced genotypes suggested rare pairings between homoeologous chromosomes. Photometric data and chromosome counts suggest backcrossing between the triploid hybrid and D. lapponica, and hence some hybrid fertility. Triploids are morphologically more similar to the tetraploids than the diploids, maybe owing to the hybrid origin of both triploids and tetraploids. The diploids and tetraploids were not more similar in the parapatric populations compared to when they occur in allopatry. This indicates that backcrossing rarely leads to introgression, or alternatively that allopatric populations are not isolated enough to prevent influx of pollen from the other species. Despite some evidence of backcrossing, our study gives few indications that widespread hybridization entails local breakdown of species boundaries. Rather, the hybrid zone may be a transient phenomenon due to intensive mowing, resulting in the opening of habitats and hence bringing the parental species into close contact.

The role of salivary androgen-binding protein in reproductive isolation between two subspecies of house mouse: Mus musculus musculus and Mus musculus domesticus

Previous behavioural studies using inbred lines have suggested that the gene (Abpa) for the alpha subunit of salivary androgen-binding protein (ABP) plays a role in prezygotic isolation between house mouse Mus musculus subspecies. We tested this hypothesis in animals from wild allopatric (121 individuals from four samples) and parapatric (320 animals from 15 samples) populations sampled on the Czech–Bavarian transect across the hybrid zone between M. m. domesticus and M. m. musculus. The study did not reveal a consistent statistically significant trend of homosubspecific preferences in individual allopatric and parapatric populations. Nonetheless, the whole pattern of preference was skewed toward homosubspecific preference mostly on the M. m. musculus side of the hybrid zone. The pattern of homosubspecific preferences was stronger for the time spent sniffing than it was for the first choice of the signal (the ratio of homosubspecific vs. heterosubspecific preferences for both sexes was 6 : 2 in allopatric and 21 : 9 in parapatric populations, while the same rates were 4 : 4 and 16 : 14 for the first choice). To the extent that Y-maze tests reflect preference under wild conditions, we suggest that this slight preference may not in itself be sufficient to impede gene flow between the two subspecies and thus act as a reproductive barrier. ABP most probably participates in a complex system of subspecies-specific recognition in the hybrid zone, but the picture is far too complex at this time to allow a conclusive evaluation of the importance of this role.

Host-related genetic differentiation in the anther smut fungus Microbotryum violaceum in sympatric, parapatric and allopatric populations of two host species Silene latifolia and S. dioica

We investigated genetic diversity in West European populations of the fungal pathogen Microbotryum violaceum in sympatric, parapatric and allopatric populations of the host species Silene latifolia and S. dioica, using four polymorphic microsatellite loci. In allopatric host populations, the fungus was highly differentiated by host species, exhibiting high values of F(ST) and R(ST), and revealed clear and distinct host races. In sympatric and parapatric populations we found significant population differentiation as well, except for one sympatric population in which the two host species grew truly intermingled. The mean number of alleles per locus for isolates from each of the host species was significantly higher in sympatric/parapatric than in allopatric populations. This suggests that either gene flow between host races in sympatry, or in case of less neutral loci, selection in a more heterogeneous host environment can increase the level of genetic variation in each of the demes. The observed pattern of host-related genetic differentiation among these geographically spread populations suggest a long-term divergence between these host races. In sympatric host populations, both host races presumably come in secondary contact, and host-specific alleles are exchanged depending on the amount of fungal gene flow.

Oviposition preference and larval performance within a diverging lineage of lycaenid butterflies

Abstract. 1. The butterfly genus Mitoura in Northern California includes three nominal species associated with four host plants having parapatric or interdigitated ranges. Genetic analyses have shown the taxa to be very closely related, and adults from all host backgrounds will mate and produce viable offspring in the laboratory. Oviposition preference and larval performance were investigated with the aim of testing the hypothesis that variation in these traits can exist in a system in which non‐ecological barriers to gene flow (i.e. geographic barriers and genetic incompatibilities) appear to be minimal.2. Females were sampled from 12 locations throughout Northern California, including sympatric and parapatric populations associated with the four different host‐plant species. Oviposition preference was assayed by confining wild‐caught females with branches of all four host species and counting the number of eggs laid on each. Offspring were reared on the same host species and two measures of larval success were taken: per cent survival and pupal weight.3. For populations associated with one of the hosts, incense cedar, the preference–performance relationship is simple: the host that females chose is the plant which results in the highest pupal weights for offspring. The preference–performance relationship for populations associated with the other hosts is more complex and may reflect different levels of local adaptation. The variation in preference and performance reported here suggests that these traits can evolve when non‐ecological barriers to gene flow are low, and that differences in these traits may be important for the evolution of reproductive isolation within Mitoura.

Evidence of reduction of gene flow between two cytotypes of Ranunculus silerifolius Lev. (Ranunculaceae) revealed with allozyme and intersimple sequence repeat polymorphisms

Gene flow between partially reproductively isolated Otaru and Matsuyama cytotypes of Ranunculus silerifolius was revealed using allozyme polymorphisms. Otaru and Matsuyama cytotypes in the parapatric population MIX were distinguishable critically by the different alleles of the Mdh-3 allozyme locus and the hybrids between both cytotypes shared both alleles of both cytotypes. The distribution pattern of the alleles of the Mdh-3 locus revealed that the gene flow did not occur between cytotypes within MIX. The value of gene flow between the two cytotypes within the parapatric population MIX (i.e. 0.503) was smaller than those between allopatric populations of the same cytotype (i.e. 2.550 or 1.700). The genetic distance between cytotypes within the parapatric population MIX was larger than those between the far distant populations of the same cytotypes. Dendrograms based on the Nei's genetic distance using the variations of allozyme markers showed that Otaru and Matsuyama cytotypes formed clusters separately.

Molecular phylogeny and plumage signal evolution in a trans Andean and circum Amazonian avian species complex

Species with fragmented distributions are particularly useful models for investigating processes underlying biological diversification in the Neotropics. The Phaeothlypis wood-warbler complex (Aves: Parulidae) is comprised of six disjunct or parapatric populations. The geographic distribution of these six populations mirrors the classic map of Neotropical areas of endemism that were originally proposed as putative Pleistocene forest refugia, but the magnitude of mitochondrial DNA divergence between these populations suggests that they are each substantially older, with origins in the late Pliocene. Phylogenetic reconstructions based on long mtDNA coding sequences show that the Guiana Shield and Atlantic Forest populations are sister lineages, and group this combined lineage and the remaining four population-specific lineages in a five-way hard polytomy. MtDNA-based phylogenetic reconstructions provide no evidence that the three populations with conspicuous yellow rump and tail feathers currently grouped as the Buff-rumped Warbler ( P. fulvicauda) form a monophyletic group. Furthermore, there is a broad discordance between mtDNA and plumage along a transect just east of the Andes, where the contact zone between highly divergent mtDNA clades is more than 1000 km north of the phenotypic hybrid zone between the bright and dark plumage forms. This discordance between mtDNA genotype and plumage phenotype is similar to patterns seen on a finer geographic scale in other avian hybrid zones and may result from asymmetric introgression of the bright plumage trait.

Taxonomy of Iberian Hoplia (Col., Scarabaeoidea, Hopliinae) based on mtDNA analysis

The morphology of some Hoplia species (Scarabaeoidea: Hopliinae) is so variable that parapatric populations have often been considered different species or subspecies. In this study we analyze the nucleotide sequences of a fragment of mitochondrial gene cytochrome c oxidase subunit I (COI) of six species and two subspecies of Palaearctic Hoplia to reexamine the species limits. Based on the analysis of sequences from COI and morphological and ecological observations, we consider Hoplia freyi Baraud to be a junior synonym of Hoplia chlorophana Erichson and H. philanthus ramburi Heyden to be a junior synonym of H. philanthus philanthus (Fuessly). However, complete resolution of relationships among H. philanthus subspecies requires the addition of sequences from genes evolving faster than COI. Phylogenetic relationships among the species studied are discussed.

Population differentiation and nuclear gene flow in the Dominican anole (Anolis oculatus)

Allele frequency data from nuclear microsatellite loci were used to investigate patterns of nuclear gene flow and population structure in the morphologically variable Dominican anole (Anolis oculatus). All six loci used proved to be highly polymorphic, with an average of 18.8 alleles per locus. Test for Hardy-Weinberg equilibrium revealed small numbers of heterozygote deficiencies at single loci in single populations and consistent patterns of increasingly significant heterozygote deficiency in global tests across populations and loci. No significant relationship between FST and patristic distances estimated from mitochondrial DNA sequences was detected and estimates of FIS were significantly higher in females than in males, indicating that gene flow may be sex-biased and mediated mainly by male migration. A highly significant correlation between linearized FST and loge (geographical distance) indicates that geographical proximity is a significant factor in the genetic structure of A. oculatus populations. However, levels of gene flow between morphologically differentiated parapatric populations are frequently seen to be relatively high. This supports the hypothesis of natural selection being the driving force behind the development and maintenance of morphological variation and shows that adaptive differentiation may be maintained despite the homogenizing influence of gene flow. Generally, the morphologically variable populations of A. oculatus are seen to be poor candidates for in situ speciation, but an exceptional case on the west coast of Dominica indicates that isolation resulting from vicariant events may lead to rapid differentiation at both mitochondrial and nuclear loci. This provides a possible mechanism for anole speciation on other Caribbean islands.

Sexual selection, reproductive isolation and the genic view of speciation

Sexual selection, reproductive isolation and the genic view of speciation

The origin of Eucalyptus vernicosa, a unique shrub eucalypt

The morphology of the Tasmanian yellow gum eucalypts varies clinally over less than 1.5 km on Mt Arrowsmith, from small shrubs on the mountaintops (Eucalyptus vernicosa), through small trees (E. subcrenulata) in sub-alpine woodland, to tall forest trees near the base of the mountain (classified as E. johnstonii or E. subcrenulata). This cline suggests a possible origin of E. vernicosa by primary differentiation. This study examines the origin of E. vernicosa on Mt Arrowsmith and two other Tasmanian mountains using four microsatellite loci. The analysis confirmed the continuous nature of the morphological variation on Mt Arrowsmith, whereas the variation on the other mountains was discontinuous. However, no corresponding pattern of clinal variation was found in microsatellite markers, with a large discontinuity between the E. vernicosa and E. subcrenulata. Eucalyptus vernicosa populations from widely separated mountains had greater genetic affinities to each other than to parapatric populations of E. subcrenulata. Morphologically intermediate phenotypes between E. vernicosa and E. subcrenulata were genetically indistinguishable from E. vernicosa. This pattern of genetic differentiation suggests that E. vernicosa evolved in allopatry and the cline on Mt Arrowsmith arose from two gene pools converging in morphology from opposite directions.

The origin of Eucalyptus vernicosa, a unique shrub eucalypt

The morphology of the Tasmanian yellow gum eucalypts varies clinally over less than 1.5 km on Mt Arrowsmith, from small shrubs on the mountaintops (Eucalyptus vernicosa), through small trees (E. subcrenulata) in sub-alpine woodland, to tall forest trees near the base of the mountain (classified as E. johnstonii or E. subcrenulata). This cline suggests a possible origin of E. vernicosa by primary differentiation. This study examines the origin of E. vernicosa on Mt Arrowsmith and two other Tasmanian mountains using four microsatellite loci. The analysis confirmed the continuous nature of the morphological variation on Mt Arrowsmith, whereas the variation on the other mountains was discontinuous. However, no corresponding pattern of clinal variation was found in microsatellite markers, with a large discontinuity between the E. vernicosa and E. subcrenulata. Eucalyptus vernicosa populations from widely separated mountains had greater genetic affinities to each other than to parapatric populations of E. subcrenulata. Morphologically intermediate phenotypes between E. vernicosa and E. subcrenulata were genetically indistinguishable from E. vernicosa. This pattern of genetic differentiation suggests that E. vernicosa evolved in allopatry and the cline on Mt Arrowsmith arose from two gene pools converging in morphology from opposite directions.

GRAPES, GALLS, AND GEOGRAPHY: THE DISTRIBUTION OF NUCLEAR AND MITOCHONDRIAL DNA VARIATION ACROSS HOST-PLANT SPECIES AND REGIONS IN A SPECIALIST HERBIVORE

Studies of patterns of molecular variation in natural populations can provide important insights into a number of evolutionary problems. Among these, the question of whether geographic factors are more important than ecological factors in promoting population differentiation and ultimately speciation has been an important and contentious area in evolutionary biology. Systems involving herbivorous insects have played a leading role in this discussion. This study examined the distribution of molecular variation in a highly specialized gall-forming insect, grape phylloxera (Daktulosphaira vitifoliae Fitch), that is found on both sympatric and allopatric host-plant species of the genus Vitis. In addition, the relationship of insects in the introduced range in the United States to ancestral populations in the native range was examined. Evidence for differentiation along host-plant lines from both nuclear (RAPD) and mitochondrial (COI) DNA was confounded with the effect of geography. Differentiation was found where hosts were allopatric or parapatric, but no evidence was found for such differentiation on two hosts, V. vulpina and V. aestivalis, that are broadly sympatric. The question of population differentiation onto these sympatric hosts can be considered to be resolved--it has not occurred in spite of a long history of association. Evidence was equivocal, but suggestive of a period of divergence in allopatry prior to reestablishment of contact, for insects associated with another host plant species, V. cinerea, found in both sympatric and parapatric populations. A low level of diversity and placement of samples collected from the grape species V. riparia at the tip of a phylogenetic tree supports the hypothesis that this host has been recently colonized from populations from the Mississippi Valley. A polyphyletic origin for biotype B grape phylloxera was supported: Although most samples collected from vineyards in the introduced range in California had similar haplotypes, they were closely related to natives on V. vulpina from the Atlantic Coast-Piedmont region. All samples collected from vineyards in Oregon and Washington were closely related to natives on V. riparia in the northern United States.

GRAPES, GALLS, AND GEOGRAPHY: THE DISTRIBUTION OF NUCLEAR AND MITOCHONDRIAL DNA VARIATION ACROSS HOST-PLANT SPECIES AND REGIONS IN A SPECIALIST HERBIVORE

Studies of patterns of molecular variation in natural populations can provide important insights into a number of evolutionary problems. Among these, the question of whether geographic factors are more important than ecological factors in promoting population differentiation and ultimately speciation has been an important and contentious area in evolutionary biology. Systems involving herbivorous insects have played a leading role in this discussion. This study examined the distribution of molecular variation in a highly specialized gall-forming insect, grape phylloxera (Daktulosphaira vitifoliae Fitch), that is found on both sympatric and allopatric host-plant species of the genus Vitis. In addition, the relationship of insects in the introduced range in the United States to ancestral populations in the native range was examined. Evidence for differentiation along host-plant lines from both nuclear (RAPD) and mitochondrial (COI) DNA was confounded with the effect of geography. Differentiation was found where hosts were allopatric or parapatric, but no evidence was found for such differentiation on two hosts, V. vulpina and V. aestivalis, that are broadly sympatric. The question of population differentiation onto these sympatric hosts can be considered to be resolved--it has not occurred in spite of a long history of association. Evidence was equivocal, but suggestive of a period of divergence in allopatry prior to reestablishment of contact, for insects associated with another host plant species, V. cinerea, found in both sympatric and parapatric populations. A low level of diversity and placement of samples collected from the grape species V. riparia at the tip of a phylogenetic tree supports the hypothesis that this host has been recently colonized from populations from the Mississippi Valley. A polyphyletic origin for biotype B grape phylloxera was supported: Although most samples collected from vineyards in the introduced range in California had similar haplotypes, they were closely related to natives on V. vulpina from the Atlantic Coast-Piedmont region. All samples collected from vineyards in Oregon and Washington were closely related to natives on V. riparia in the northern United States.

Gene flow and differential mortality in a contact zone between two Albinaria species (Gastropoda; Clausiliidae)

This paper reports on the disruption of normally effective ecological and behavioural barriers, at a contact zone on Monemvasia peninsula (Peloponnese, Greece), between parapatric populations of the land snail species Albinaria discolor and Albinaria campylauchen. Detected outcomes were the increase of gene flow between these two species at the contact zone, the occurrence of rare alleles, as well as the occurrence of morphologically and ethologically intermediate A. campylauchen specimens. Furthermore, there was high genetic variability along with deficiency of heterozygotes, probably due to inbreeding. Additionally, the study of mortality of these populations, during the adverse summer aestivation period, indicated that A. campylauchen individuals with an inappropriate combination of morphological and behavioural characteristics suffered heavily. The maladaptation and disadvantage of these specimens revealed the possible action of a postzygotic isolation mechanism between these two morphologically, molecularly and electrophoretically distinct species, that can, however, mate under laboratory conditions. Finally, the above situation is discussed in terms of exogenous versus endogenous selection.

Gene flow and differential mortality in a contact zone between two Albinaria species (Gastropoda; Clausiliidae)

This paper reports on the disruption of normally effective ecological and behavioural barriers, at a contact zone on Monemvasia peninsula (Peloponnese, Greece), between parapatric populations of the land snail species Albinaria discolor and Albinaria campylauchen. Detected outcomes were the increase of gene flow between these two species at the contact zone, the occurrence of rare alleles, as well as the occurrence of morphologically and ethologically intermediateA. campylauchen specimens. Furthermore, there was high genetic variability along with deficiency of heterozygotes, probably due to inbreeding. Additionally, the study of mortality of these populations, during the adverse summer aestivation period, indicated that A. campylauchen individuals with an inappropriate combination of morphological and behavioural characteristics suffered heavily. The maladaptation and disadvantage of these specimens revealed the possible action of a postzygotic isolation mechanism between these two morphologically, molecularly and electrophoretically distinct species, that can, however, mate under laboratory conditions. Finally, the above situation is discussed in terms of exogenous versus endogenous selection.