Ecological genomics of Anopheles gambiae along a latitudinal cline: a population-resequencing approach

The association between fitness-related phenotypic traits and an environmental gradient offers one of the best opportunities to study the interplay between natural selection and migration. In cases in which specific genetic variants also show such clinal patterns, it may be possible to uncover the mutations responsible for local adaptation. The malaria vector, Anopheles gambiae, is associated with a latitudinal cline in aridity in Cameroon; a large inversion on chromosome 2L of this mosquito shows large differences in frequency along this cline, with high frequencies of the inverted karyotype present in northern, more arid populations and an almost complete absence of the inverted arrangement in southern populations. Here we use a genome resequencing approach to investigate patterns of population divergence along the cline. By sequencing pools of individuals from both ends of the cline as well as in the center of the cline- where the inversion is present in intermediate frequency- we demonstrate almost complete panmixia across collinear parts of the genome and high levels of differentiation in inverted parts of the genome. Sequencing of separate pools of each inversion arrangement in the center of the cline reveals large amounts of gene flux (i.e., gene conversion and double crossovers) even within inverted regions, especially away from the inversion breakpoints. The interplay between natural selection, migration, and gene flux allows us to identify several candidate genes responsible for the match between inversion frequency and environmental variables. These results, coupled with similar conclusions from studies of clinal variation in Drosophila, point to a number of important biological functions associated with local environmental adaptation.     

Diverse spore rains and limited local exchange shape fern genetic diversity in a recently created habitat colonized by long-distance dispersal

Background and Aims

Populations established by long-distance colonization are expected to show low levels of genetic variation per population, but strong genetic differentiation among populations. Whether isolated populations indeed show this genetic signature of isolation depends on the amount and diversity of diaspores arriving by long-distance dispersal, and time since colonization. For ferns, however, reliable estimates of long-distance dispersal rates remain largely unknown, and previous studies on fern population genetics often sampled older or non-isolated populations. Young populations in recent, disjunct habitats form a useful study system to improve our understanding of the genetic impact of long-distance dispersal.

Methods

Microsatellite markers were used to analyse the amount and distribution of genetic diversity in young populations of four widespread calcicole ferns (Asplenium scolopendrium, diploid; Asplenium trichomanes subsp. quadrivalens, tetraploid; Polystichum setiferum, diploid; and Polystichum aculeatum, tetraploid), which are rare in The Netherlands but established multiple populations in a forest (the Kuinderbos) on recently reclaimed Dutch polder land following long-distance dispersal. Reference samples from populations throughout Europe were used to assess how much of the existing variation was already present in the Kuinderbos.

Key Results

A large part of the Dutch and European genetic diversity in all four species was already found in the Kuinderbos. This diversity was strongly partitioned among populations. Most populations showed low genetic variation and high inbreeding coefficients, and were assigned to single, unique gene pools in cluster analyses. Evidence for interpopulational gene flow was low, except for the most abundant species.

Conclusions

The results show that all four species, diploids as well as polyploids, were capable of frequent long-distance colonization via single-spore establishment. This indicates that even isolated habitats receive dense and diverse spore rains, including genotypes capable of self-fertilization. Limited gene flow may conserve the genetic signature of multiple long-distance colonization events for several decades.     

A latitudinal cline in a Drosophila clock gene.

The clock gene period determines biological rhythmicity in Drosophila melanogaster and encodes a protein characterized by an alternating series of threonine-glycine pairs. The minisatellite region encoding the threonine-glycine repeat is polymorphic in length in natural Drosophila melanogaster populations. In this paper we report the geographical analysis of this polymorphism within Europe and North Africa. A robust clinal pattern is observed along a north-south axis. We suggest the possibility that the length polymorphism could be maintained by thermal selection because the threonine-glycine region has been shown to provide thermostability to the circadian phenotype.     

Population dynamics ofGlaux maritima (L.) along a distributional cline

Population fluctuations ofGlaux maritima, along a transect on a Baltle sea shore meadow, were recorded between 1979 and 1983. A bimodal distribution in numbers along the transect reflects the variation in factors regulating numbers: The two maintenance systems of the species, vegetative propagation and sexual reproduction play different roles. Vegetative propagation is fast and responds quickly to variations in the environment. The seeds germinate in strongly fluctuating temperatures which are triggered by disturbances such as flooding, damaging the vegetation.     

Salamander evolution across a latitudinal cline in gape-limited predation risk

General predictions of community dynamics require that insights derived from local habitats can be scaled up to explain phenomena across geographic scales. Across these larger spatial extents, adaptation can play an increasing role in determining the outcome of species interactions. If local adaptation is common, then our ability to generalize measures of species interaction strength across communities will be limited without an additional understanding of the genetic variation underlying interaction traits. In the context of predator–prey interactions, prey individuals commonly are expected to reduce risky foraging behaviors and subsequent growth under predation threat. However, rapid growth into a large body size can defend against gape-limited predators, creating a tradeoff between increased predation risk due to elevated foraging activity and decreased predation risk due to large size. Here I combine field observations, natural selection experiments, and common garden assays to understand potential adaptations of spotted salamander Ambystoma maculatum larvae to gape-limited and gape-unconstrained predators. Field observations and natural selection trials suggested antagonistic selection on prey body size among ponds dominated by gape-limited predator salamanders A. opacum and gape-unconstrained beetle larvae Dytiscus . In common garden experiments, prey from sites with high gape-limited predation risk grew larger than those from other sites, suggesting the evolution of rapid growth into a prey size refuge. Larvae from all sites grew to a large size when exposed to the gape-limited N. viridescens predator's kairomones. Hence, induced rapid growth into a size refuge may be an adaptive response to gape-limited predation risk. Results point to an important role for cross-community generalizations based on functional classifications of predators by their gape constraints and inter-site genetic variation in prey growth rates and behaviors.     

Life history adaptation along a latitudinal cline in the water strider Aquarius remigis (Heteroptera: Gerridae)

We addressed the general hypothesis that life history differences among eastern populations of the North American water strider, Aquarius remigis (Heteroptera: Gerridae), along a north-south gradient are manifestations of genetic differentiation due to natural selection. We raised offspring of two field-caught populations from each of three latitudes in a common laboratory environment at 20° C and two photoperiods. Nearly all Quebec (PQ) individuals (ca. 46° N) entered diapause to reproduce the following spring (univoltine life cycle), while intermediate proportions of New York (NY; ca. 43° N) and New Jersey (NJ; ca. 41° N) individuals reproduced directly, producing a second generation (bivoltine life cycle). PQ females were smaller, developed faster, and laid smaller eggs than NY and NJ individuals; NY and NJ populations differed little in these variables. NY females had longer life spans than either PQ or NJ females, but lower oviposition rates. Total reproductive output did not differ across latitudes. Photoperiod affected body length, development time, and reproductive pathway, resulting in a latitude by environmental interaction. PQ individuals reproduced directly under 15L : 9D (summer) conditions only, while the NY and NJ populations exhibited more direct reproduction under 13L : 11D (spring or fall) conditions. Some life history characters of the NY and NJ populations displayed the higher variability indicative of phenological transition zones. These results indicate local adaptation of populations to long-term climatic patterns. Water striders appear to adapt to longer seasons by extending development, growing larger, and breeding directly. Larger body size and extended or rapid development are associated with bivoltinism and increase in egg size, but not necessarily with higher fecundity or oviposition rate. The phenological transition zone appears to be unrelated to a transition zone a little further south established by allozyme data and morphology, as all populations studied here could be electrophoretically identified as northern "type".     

The swimbladder nematode Anguillicola crassus in the European eel Anguilla anguilla and the Japanese eel Anguilla japonica: differences in susceptibility and immunity between a recently colonized host and the original host

The swimbladder nematode Anguillicola crassus originates from Asia where it is a parasite of the Japanese eel Anguilla japonica. After its introduction to Europe about 25 years ago, the parasite spread rapidly within the indigenous populations of the European eel Anguilla anguilla and subsequently the prevalence and mean intensity appeared to stabilize. Under experimental and aquaculture conditions the na?ve new host appears to be more susceptible to A. crassus compared to the original host. Both eel species develop a immune response against A. crassus. The antibody response is well characterized for the European eel, but poorly characterized for the Japanese eel. It remains unclear if antibodies have any protective function against A. crassus. Encapsulation of larvae of A. crassus can be observed in naturally infected European eels. However, encapsulation of larvae following experimental infection has not been detected in European eels, but only in Japanese eels. Reinfection experiments and intraperitoneal injection of A. crassus homogenates failed to demonstrate the development of acquired immunity in European eels. Immunization with irradiated third stage larvae provided preliminary evidence for acquired immunity against A. crassus in the Japanese eel, but not in the European eel.     

Population genomics reveals differences in genetic structure between two endemic arboreal rodent species in threatened cloud forest habitat

Mammal Research - Genomic tools are now commonly used to assess the genetic diversity and genetic structure of species and populations, and they provide the ability to describe and address the...     

Ontogenetic changes in genetic variances of age-dependent plasticity along a latitudinal gradient

The expression of phenotypic plasticity may differ among life stages of the same organism. Age-dependent plasticity can be important for adaptation to heterogeneous environments, but this has only recently been recognized. Whether age-dependent plasticity is a common outcome of local adaptation and whether populations harbor genetic variation in this respect remains largely unknown. To answer these questions, we estimated levels of additive genetic variation in age-dependent plasticity in six species of damselflies sampled from 18 populations along a latitudinal gradient spanning 3600 km. We reared full sib larvae at three temperatures and estimated genetic variances in the height and slope of thermal reaction norms of body size at three points in time during ontogeny using random regression. Our data show that most populations harbor genetic variation in growth rate (reaction norm height) in all ontogenetic stages, but only some populations and ontogenetic stages were found to harbor genetic variation in thermal plasticity (reaction norm slope). Genetic variances in reaction norm height differed among species, while genetic variances in reaction norm slope differed among populations. The slope of the ontogenetic trend in genetic variances of both reaction norm height and slope increased with latitude. We propose that differences in genetic variances reflect temporal and spatial variation in the strength and direction of natural selection on growth trajectories and age-dependent plasticity. Selection on age-dependent plasticity may depend on the interaction between temperature seasonality and time constraints associated with variation in life history traits such as generation length.     

Temperature-induced oviposition in the brachyuran crab Cancer setosus along a latitudinal cline: Aquaria experiments and analysis of field-data

Ovigerous females of Cancer setosus are present year-round throughout most of its wide range along the Peruvian/Chilean Pacific coast (2°S-46°S). However, their number of egg-masses produced per year remains speculative and as such has neither been considered in latitudinal comparisons of reproduction, nor for its fisheries management. In order to reveal the effect of temperature on egg-mass production and egg-development, female C. setosus were held in through-flow aquaria under natural seasonal temperature conditions (16-23 °C) in Antofagasta (23°S), Northern Chile (05/2005-03/2006; 10 months), and at three constant temperatures (12, 16, 19 °C) in Puerto Montt (41°S), Central Southern Chile (09/2006-02/2007; 5 months). Female crabs uniformly produced up to 3 viable egg-masses within 4 1/2 months in Antofagasta and in Puerto Montt (at 19 °C). The second egg-mass was observed 62.5 days (± 7.6; N = 7) after the oviposition of the first clutch and a third egg-mass followed 73.5 days (± 12.5; N = 11) later in Antofagasta (at 16-23 °C). Comparably, a second oviposition took place 64.4 days (± 9.8, N = 5) after the first clutch and a third, 67.0 days (± 2.8, N = 2), thereafter, at 19 °C in Puerto Montt. At the two lower temperatures (16 and 12 °C) in Puerto Montt a second egg-mass was extruded after 82.8 days (± 28.9; N = 4) and 137 days (N = 1), respectively. The duration of egg-development from oviposition until larval hatching decreased from 65 days at 12.5 °C to 22.7 days at the observed upper temperature threshold of 22 °C. Based on the derived relationship between temperature and the duration of egg-development (y = 239.3175e^{− 0.107x}; N = 21, r² = 0.83) and data on monthly percentages of ovigerous females from field studies, the annual number of egg-masses of C. setosus was calculated. This analysis revealed an annual output of about one egg-mass close to the species northern and southern distributional limits in Casma (9°S) and Ancud (43°S), respectively, while at Coquimbo (29°S) about two and in Concepción (36°S) more than 3 egg-masses are produced per year.     

Intraspecific and interspecific adaptive latitudinal cline in Brassicaceae seed oil traits

Premise of the Study

Nearly all seed plants rely on stored seed reserves before photosynthesis can commence. Natural selection for seed oil traits must have occurred over 319 million years of evolution since the first seed plant ancestor. Accounting for the biogeographic distribution of seed oil traits is fundamental to understanding the mechanisms of adaptive evolution in seed plants. However, the evolution of seed oils is poorly understood. We provide evidence of the adaptive nature of seed oil traits at the intraspecific and interspecific levels in Brassicaceae—an oilseed‐rich and economically important plant family.

Methods

Univariate statistics, Pearson's correlation, multiple regression, generalized linear mixed model analysis, and phylogenetic autocorrelation tests on seed oil traits of 360 accessions of Arabidopsis thaliana and 216 Brassicaceae species helped provide evidence of the adaptive nature of seed oil traits.

Key Results

At higher latitudes, both seed oil content and unsaturated fatty acids have selective advantages in Arabidopsis thaliana (intraspecific‐level), while only unsaturated fatty acids have selective advantages across 216 Brassicaceae species (interspecific‐level). The seed oil patterns fit within the theoretical framework of the gradient model. Seed oil content increases significantly from temperate to subtropical to tropical regions in Brassicaceae herbs. Absence of phylogenetic signals for seed oil traits and high seed oil content in four tribes of Brassicaceae were observed.

Conclusions

Multiple seed oil traits are adaptive in nature and follow a gradient model. Consistent evolutionary patterns of seed oil traits were observed at the intraspecific and interspecific levels in Brassicaceae. Seed oil traits change with latitude and across biomes, suggesting selection. The absence of a phylogenetic signal for seed oil traits and the occurrence of high seed oil content in four Brassicaceae tribes provides evidence of the adaptive nature of seed oil traits in Brassicaceae.     

Avian Clock gene polymorphism: evidence for a latitudinal cline in allele frequencies

In comparison with most animal behaviours, circadian rhythms have a well-characterized molecular genetic basis. Detailed studies of circadian clock genes in 'model' organisms provide a foundation for interpreting the functional and evolutionary significance of polymorphic circadian clock genes found within free-living animal populations. Here, we describe allelic variation in a region of the avian Clock orthologue which encodes a functionally significant polyglutamine repeat (ClkpolyQcds), within free-living populations of two passerine birds, the migratory bluethroat (Luscinia svecica) and the predominantly nonmigratory blue tit (Cyanistes caeruleus). Multiple ClkpolyQcds alleles were found within populations of both species (bluethroat: 12 populations, 7 alleles; blue tit: 14 populations, 9 alleles). Some populations of both species were differentiated at the ClkpolyQcds locus as measured by F(ST) and R(ST) values. Among the blue tit, but not bluethroat populations, we found evidence of latitudinal clines in (i) mean ClkpolyQcds repeat length, and (ii) the proportions of three ClkpolyQcds genotype groupings. Parallel analyses of microsatellite allele frequencies, which are considered to reflect selectively neutral processes, indicate that interpopulation allele frequency variation at the ClkpolyQcds and microsatellite loci does not reflect the same underlying demographic processes. The possibility that the observed interpopulation ClkpolyQcds allele frequency variation is, at least in part, maintained by selection for microevolutionary adaptation to photoperiodic parameters correlated with latitude warrants further study.     

Analysis of genetic diversity in a peatland specialist butterfly suggests an important role for habitat quality and small habitat patches

Understanding effects of habitat and landscape features on genetic variation is a prerequisite for the development of habitat and landscape management strategies aimed at conserving genetic diversity. While there has been considerable research on the effects of landscape structure on the genetics of populations, a recent review identified key biases in this body of work. The majority of landscape genetic studies investigate the intervening matrix’s influence on differentiation and gene flow among populations. Although characteristics of local habitat patches may be important determinants of genetic diversity, fewer studies have examined these relationships. Here we use node- and neighbourhood-based approaches to analyze correlates of genetic diversity in the bog copper (Lycaena epixanthe), a specialist butterfly endemic to temperate Nearctic peatlands that is threatened in parts of its range. Based on 190 repeatable and polymorphic amplified fragment length polymorphism loci, we found that genetic diversity was higher in habitat patches that were smaller and surrounded by more open water. Our results indicate that valuing small peatlands and preserving the surrounding water table may be important for conservation of genetic diversity in this highly specialized species. Our study highlights the importance of variables affecting habitat quality for conservation genetics.     

Population structure and colour variation of the cichlid fishes Labeotropheus fuelleborni Ahl along a recently formed archipelago of rocky habitat patches in southern Lake Malawi

Extremely fine-scale genetic partitioning has recently been detected among populations of Lake Malawi''s rock-dwelling cichlids through the study of microsatellite loci. Understanding the mechanisms of genetic differentiation that operate in this rapidly speciating group requires further investigation of the geographic patterns of gene flow and the congruence between morphological and genetic divergence. In pursuit of this goal, genetic variation at four microsatellite loci and variation in male breeding coloration were examined in several populations of Labeotropheus fuelleborni from southern Lake Malawi. Significant genetic differentiation exists among populations (overall F_ST = 0.063; p = 0.0002). While migration appears unrestricted within continuous rocky patches, deep waters and sandy bays more than 2 km wide act as strong barriers to gene flow. Dispersal of L. fuelleborni appears to follow a stepping-stone model in which the distribution of habitats often constrains migration to one dimension. It is hypothesized that clinal colour variation in the study area has resulted from the secondary contact of divergent lineages, although reproductive isolation between colour variants is not apparent. Relative to shoreline populations, reduced levels of gene flow among populations inhabiting isolated, deep-water islands provides greater opportunities for drift, adaptation to local conditions, or sexual selection to effect genetic differentiation in this species.     

Genetic differentiation across a latitudinal gradient in two co-occurring butterfly species: revealing population differences in a context of climate change

Genetic differentiation within a species' range is determined by natural selection, genetic drift, and gene flow. Selection and drift enhance genetic differences if populations are sufficiently isolated, while gene flow precludes differentiation and local adaptation. Over large geographical areas, these processes can create a variety of scenarios, ranging from admixture to a high degree of population differentiation. Genetic differences among populations may signal functional differences within a species' range, potentially leading to population or ecotype-specific responses to global change. We investigated differentiation within the geographical range of two butterfly species along a broad latitudinal gradient. This gradient is the primary axis of climatic variation, and many ecologists expect populations at the poleward edge of this gradient to expand under climate change. Our study species inhabit a shared ecosystem and differ in body size and resource specialization; both also find their poleward range limit on an island. We find evidence for divergence of peripheral populations from the core in both taxa, suggesting the potential for genetic distinctiveness at the leading edge of climate change. We also find differences between the species in the extent of peripheral differentiation with the smaller and more specialized species showing greater population divergence (microsatellites and mtDNA) and reduced gene flow (mtDNA). Finally, gene flow estimates in both species differed strongly between two marker types. These findings suggest caution in assuming that populations are invariant across latitude and thus will respond as a single ecotype to climatic change.     

Origin and decay of the P element-associated latitudinal cline in Australian Drosophila melanogaster

The latitudinal cline in P transposable element-associated characteristics in eastern Australian populations of Drosophila melanogaster has changed between 1986 and 1991–1994. New collections were made in 1991–1994 from localities along the eastern coast of Australia. P element-associated properties of 256 isofemale lines from 43 localities were evaluated using gonadal dysgenesis and/or singed-weak hypermutability assays. The overall results indicate that both P activity and P susceptibility have declined, with all populations showing a tendency towards a state with little P activity potential but with P repressor function (neutral or ‘Q’). P repressor function is strong in all populations except some of the most southerly. P activity potential peaks at about 27° SLat, and drops off to the south (as in 1983–1986 collections) and to the north (in contrast to 1983–1986 collections); thus the cline is no longer a simple P-to-Q-to-M pattern from north to south, but is now Q-P-Q-M. A mtDNA RFLP that putatively distinguishes North American and European populations varies in frequency among the populations but the frequency does not vary clinally with latitude, ruling out massive introductions from North America and Europe as causing the cline. This revised version was published online in July 2006 with corrections to the Cover Date.     

A morphological cline in Eucalyptus: a genetic perspective

The putative hybrid zone between Eucalyptus populnea and E. brownii is examined using morphological and molecular techniques. This species complex displays continuous morphological variation across the study area, which has been previously interpreted as the product of hybridization between allopatric species. A microsatellite analysis indicates that there was little genetic structuring across the morphological cline and only low levels of population differentiation. The nested clade analysis of the JLA+ region of the chloroplast DNA (cpDNA) indicates that the geographical distribution of cpDNA haplotypes is unlikely to be the result of historical hybridization events, and that restricted seed-mediated gene flow with isolation by distance is responsible for the phylogeographical distribution. A more plausible explanation for the origin and persistence of the morphological cline is that the process of continuous morphological diversification has been promoted by a directional selection gradient. This study addresses species status within Eucalyptus and the belief that hybridization is widespread and is an important process in the group's evolution.     

Relaxed circadian rhythm in zooplankton along a latitudinal gradient

To test whether aquatic invertebrates are able to adjust their diel migratory cycle to different day length and presence of predators, we performed standardized enclosure experiments in shallow lakes at four different latitudes from southern Spain, with strong night–day cycles, to Finland where daylight is almost continuous during summer. We show here that nearly continuous daylight at high latitudes causes a relaxation in diel migratory behaviour in zooplankton irrespective of predation risk. At lower latitudes, however, similar conditions lead to pronounced diel rhythms in migration. Hence, zooplankton may show local behavioural adaptations in their circadian rhythm. They are also able to make risk assessments as to whether diel migration is beneficial or not, manifested in a lack of diel migration at near constant daylight, irrespective of predator presence. Our results provide an additional explanation to previous knowledge regarding diel migrations among aquatic invertebrates by showing that both physical (light) and biological (predation) factors may affect the migratory behaviour.     

Inbreeding uncovers fundamental differences in the genetic load affecting male and female fertility in a butterfly

Inbreeding depression is most pronounced for traits closely associated with fitness. The traditional explanation is that natural selection eliminates deleterious mutations with additive or dominant effects more effectively than recessive mutations, leading to directional dominance for traits subject to strong directional selection. Here we report the unexpected finding that, in the butterfly Bicyclus anynana, male sterility contributes disproportionately to inbreeding depression for fitness (complete sterility in about half the sons from brother-sister matings), while female fertility is insensitive to inbreeding. The contrast between the sexes for functionally equivalent traits is inconsistent with standard selection arguments, and suggests that trait-specific developmental properties and cryptic selection play crucial roles in shaping genetic architecture. There is evidence that spermatogenesis is less developmentally stable than oogenesis, though the unusually high male fertility load in B. anynana additionally suggests the operation of complex selection maintaining male sterility recessives. Analysis of the precise causes of inbreeding depression will be needed to generate a model that reliably explains variation in directional dominance and reconciles the gap between observed and expected genetic loads carried by populations. This challenging evolutionary puzzle should stimulate work on the occurrence and causes of sex differences in fertility load.