Moose body mass variation revisited: disentangling effects of environmental conditions and genetics

Large-scale geographical variation in phenotypic traits within species is often correlated to local environmental conditions and population density. Such phenotypic variation has recently been shown to also be influenced by genetic structuring of populations. In ungulates, large-scale geographical variation in phenotypic traits, such as body mass, has been related to environmental conditions and population density, but little is known about the genetic influences. Research on the genetic structure of moose suggests two distinct genetic lineages in Norway, structured along a north-south gradient. This corresponds with many environmental gradients, thus genetic structuring provides an additional factor affecting geographical phenotypic variation in Norwegian moose. We investigated if genetic structure explained geographical variation in body mass in Norwegian moose while accounting for environmental conditions, age and sex, and if it captured some of the variance in body mass that previously was attributed to environmental factors. Genetic structuring of moose was the most important variable in explaining the geographic variation in body mass within age and sex classes. Several environmental variables also had strong explanatory power, related to habitat diversity, environmental seasonality and winter harshness. The results suggest that environmental conditions, landscape characteristics, and genetic structure should be evaluated together when explaining large-scale patterns in phenotypic characters or life history traits. However, to better understand the role of genetic and environmental effects on phenotypic traits in moose, an extended individual-based study of variation in fitness-related characters is needed, preferably in an area of convergence between different genetic lineages.     

Present genetic structure revealed by microsatellites reflects recent history of the Finnish moose (Alces alces)

Genetic structures of Holarctic species are largely formed by Pleistocene colonisation history, dispersal capacity and interactions between biotic and abiotic factors, even though the human impact can also be significant. The Holarctic moose (Alces alces) arrived in Fennoscandia around 9,000–8,000 years ago, and it has been exploited by humans ever since. During the last 400 years, the Finnish moose population has suffered from several population declines, and even local and regional extirpations have occurred. The purpose of the present study is to describe the genetic variation and population structure of the Finnish moose in order to clarify how historical events and human exploitation have influenced the present-day genetic patterns. Altogether 130 moose individuals from seven sampling sites in Finland were analysed at ten microsatellite loci. A variety of population genetic and coalescent-based methods was applied. The Finnish moose population was found to be divided into southern and northern subpopulations with additional lower hierarchical genetic structure. The estimated time of divergence between these two subpopulations was about 96–238 years ago. In addition, an isolation-by-distance pattern was discovered.     

Morphological and Genetic Divergences in a Coral Reef Damselfish, Pomacentrus coelestis

Population differentiation is one of the main topics in evolutionary biology. Except the exploration of color variation, few studies focused on morphological divergences among populations of coral reef fishes. In this work, we studied morphological and genetic differentiation among populations of the damselfish, Pomacentrus coelestis, in the northwestern Pacific Ocean. The shapes of the mandible and the premaxilla were explored using geometric morphometric methods and the genetic structure was investigated using microsattelites. Various tests revealed significant shape variation among most P. coelestis populations for both skeletal units. Morphological variation of the mandible accompanies a genetic break between populations of mainland Japan and Okinawa-Taiwan. However, Mantel and Procrustes tests revealed no congruence between morphological and genetic structures. We illustrate that phenotypic plasticity and adaptive divergence are potential evolutionary mechanisms underlying shape difference among P. coelestis populations. An ecomorphological approach suggests that various diet could be related to shape variation of oral jaws.     

Population at the edge: increased divergence but not inbreeding towards northern range limit in Acer campestre

Ecological conditions shape natural distribution of plants. Populations are denser in optimal habitats but become more fragmented in the areas of suboptimal environmental conditions. Usually, fragmentation increases towards the limits of species distribution. Fragmented populations are often characterised by decreased genetic variation, and this effect is frequent in peripheral populations, mostly due to the reduced effective population size. Interestingly, the genetic consequences of fragmentation seem to be relatively weak in forest trees. Using microsatellite markers, we assessed the impact of population fragmentation on the genetic structure of a European tree species Acer campestre. Within the study area, this medium-size wind-dispersed and insect-pollinated tree reveals a gradual decrease in population density towards the northern range limit. Over the distance of 150 km, we detected the significant decrease in allelic richness, heterozygosity as well as an increase in the rate of population divergence along with latitude. On the other hand, we failed to show that the observed patterns of genetic structure result from the variation in population densities. Moreover, inbreeding levels revealed no association with both density and geographic location, suggesting that pollen limitation does not occur, even at the range margin. As we showed that there is no difference in a dispersal scale between low- and high-density populations in the study species, we argue that the genetic structure is a result of postglacial recolonization. However, unlike many other forest trees, A. campestre showed the sharp latitudinal genetic pattern at a very restricted spatial scale. Limited dispersal and high fragmentation are likely the reasons.     

Genotype–environment interaction and the ontogeny of diet-induced phenotypic plasticity in size and shape of Melanoplus femurrubrum (Orthoptera: Acrididae)

The developmental origin of phenotypic plasticity in morphological shape can be attributed to environment-specific changes in growth of overall body size, localized growth of a morphological structure or a combination of both. I monitored morphological development in the first four nymphal instars of grasshoppers (Melanoplus femurrubrum) raised on two different plant diets to determine the ontogenetic origins of diet-induced phenotypic plasticity and to quantify genetic variation for phenotypic plasticity. I measured diet-induced phenotypic plasticity in body size (tibia length), head size (articular width and mandible depth) and head shape (residual articular width and residual mandible depth) for grasshoppers from 37 full-sib families raised on either a hard plant diet (Lolium perenne) or a soft plant diet (Trifolium repens). By the second to third nymphal instar, grasshoppers raised on a hard plant diet had significantly smaller mean tibia length and greater mean residual articular width (distance between mandibles adjusted for body size) compared with full-sibs raised on a soft plant diet. However, there was no significant phenotypic plasticity in mean unadjusted articular width and mandible depth, and in mean residual mandible depth. At the population level, development of diet-induced phenotypic plasticity in grasshopper head shape is mediated by plastic changes in allocation to tissue growth that maintain growth of head size on hard, low-nutrient diets while reducing growth of body size. Within the population, there was substantial variation in the plasticity of growth trajectories since different full-sib families developed phenotypic plasticity of residual articular width through different combinations of head and body size growth. Genetic variation for diet-induced phenotypic plasticity of residual articular width, residual mandible depth and tibia length, as estimated by genotype–environment interaction, exhibited significant fluctuation through ontogeny (repeated measures MANOVA , family × plant × instar, P < 0.01). For example, there was significant genetic variation for phenotypic plasticity of residual articular width in the third nymphal instar, but not earlier or later in ontogeny. The observed patterns of genetic variation are discussed with reference to short-term constraints and the evolution of phenotypic plasticity.     

Genetic discontinuities in a continuously distributed and highly mobile ungulate,the Norwegian moose

Many species with currently continuously distributed populations have histories of geographic range shifts and successive shifts between decline or fragmentation, growth and spatial expansion. The moose (Alces alces) colonised Scandinavia after the last ice age. Historic records document a high abundance and a wide distribution across Norway in the middle ages, but major decline and fragmentation in the eighteenth and nineteenth centuries. After growth and expansion during the twentieth century, the Norwegian population is currently abundant and continuously distributed. We examined the distribution of genetic variation, differentiation and admixture in Norwegian moose, using 15 microsatellites. We assessed whether admixture has homogenised the population or if there are any genetic structures or discontinuities that can be related to recent or ancient shifts in demography or distribution. The Bayesian clustering algorithm STRUCTURE without any spatial information showed that there is currently a genetic dichotomy dividing the population into one southern and one northern subpopulation. Including spatial information, the Bayesian clustering algorithm TESS, which considers gradients of genetic variation and spatial autocorrelation, suggests that the population is divided into three subpopulations along a latitudinal axis, the southern one identical to the one identified with STRUCTURE. Present convergence zones of high admixture separate the identified subpopulations, which are delimited by genetic discontinuities corresponding to geographic barriers against dispersal, e.g. wide fiords and mountain ranges. The distribution of the subpopulations is supported by spatial autocorrelation analysis. However, some loci are not in Hardy–Weinberg equilibrium and the STRUCTURE analysis suggests that a lower hierarchical structure may exist within the southernmost subpopulation. No bottlenecks or founder events are indicated by the levels of genetic variation, rather a high degree of private alleles in the northern subpopulations indicates introgression. Coalescent-based Approximate Bayesian Computation estimates unambiguously suggest that the genetic structure is a result of an ancient divergence event and a more recent admixture event a few centuries ago. This indicates that the central Scandinavian subpopulation constitutes a relatively recent convergence zone of secondary contact.     

Ecogeographic analysis of morphological and life-history variation in the Italian treefrog

We describe the spatial pattern of variation in body size, body shape, and adult population age structure of the Italian treefrog (Hyla intermedia). By means of a non-parametric test of matrix association (the Partial Mantel Test), we investigate the role of climate and geography in explaining the patterns of phenotypic variation. Body size is the most important source of morphometric variation, both at intra- and inter-populational levels. Body shape, despite its secondary role in explaining variation, still maintains high discriminative power among populations. Age structure differs significantly among populations, since body size correlates positively to age, these differences partly explain geographic variation of body size. The patterns of variation in both age and body size are congruent with climate variation, suggesting causal relationship. However, we find no evidence for adaptive explanations and suggest that climate-induced demographically differential survivorship might be the proximate cause responsible for the associations observed. Unlike body size, body shape varies congruently with the pattern of between-population geographic distances, which we show to be highly correlated with their genetic distances, thus suggesting isolation by distance as the proximate cause of the association.     

Shell morphology and color of the subtidal whelk Buccinum undatum exhibit fine‐scaled spatial patterns

Geographical patterns in morphology can be the result of divergence among populations due to neutral or selective changes and/or phenotypic plasticity in response to different environments. Marine gastropods are ideal subjects on which to explore these patterns, by virtue of the remarkable intraspecific variation in life‐history traits and morphology often observed across relatively small spatial scales. The ubiquitous N‐Atlantic common whelk (Buccinum undatum) is well known for spatial variation in life‐history traits and morphology. Previous studies on genetic population structure have revealed that it exhibits significant differentiation across geographic distances. Within Breiðafjörður Bay, a large and shallow bay in W‐Iceland, genetic differentiation was demonstrated between whelks from sites separated by just 20 km. Here, we extended our previous studies on the common whelk in Breiðafjörður Bay by quantifying phenotypic variation in shell morphology and color throughout the Bay. We sought to test whether trait differentiation is dependent on geographic distance and/or environmental variability. Whelk in Breiðafjörður Bay displayed fine‐scale patterns of spatial variation in shape, thickness, and color diversity. Differentiation increased with increasing distance between populations, indicating that population connectivity is limited. Both shape and color varied along a gradient from the inner part of the bay in the east to the outer part in the west. Whelk shells in the innermost part of Breiðafjörður Bay were thick with an elongate shell, round aperture, and low color diversity, whereas in the outer part of the bay the shells were thinner, rounder, with a more elongate aperture and richer color diversity. Significant site‐specific difference in shell traits of the common whelk in correlation with environmental variables indicates the presence of local ecotypes and limited demographic connectivity.     

INTEGRATIVE TESTING OF HOW ENVIRONMENTS FROM THE PAST TO THE PRESENT SHAPE GENETIC STRUCTURE ACROSS LANDSCAPES

Tests of the genetic structure of empirical populations typically focus on the correlative relationships between population connectivity and geographic and/or environmental factors in landscape genetics. However, such tests may overlook or misidentify the impact of candidate factors on genetic structure, especially when connectivity patterns differ between past and present populations because of shifting environmental conditions over time. Here we account for the underlying demographic component of population connectivity associated with a temporarily dynamic landscape in tests of the factors structuring population genetic variation in an Australian lizard, Lerista lineopunctulata, from 24 nuclear loci. Correlative tests did not support significant effect from factors associated with a static contemporary landscape. However, spatially explicit demographic modeling of genetic differentiation shows that changes in environmental conditions (as estimated from paleoclimatic data) and corresponding distributional shifts from the past to present landscape significantly structures genetic variation. Results from model‐based inference (i.e., from an integrative modeling approach that generates spatially explicit expectations that are tested with approximate Bayesian computation) contrasts with those from correlative analyses, highlighting the importance of expanding the landscape genetic perspective to tests the links between pattern and process, revealing how factors shape patterns of genetic variation within species.     

Living on the edge: the role of geography and environment in structuring genetic variation in the southernmost populations of a tropical oak

Understanding the factors determining genetic diversity and structure in peripheral populations is a long‐standing goal of evolutionary biogeography, yet little empirical information is available for tropical species. In this study, we combine information from nuclear microsatellite markers and niche modelling to analyse the factors structuring genetic variation across the southernmost populations of the tropical oak Quercus segoviensis. First, we tested the hypothesis that genetic variability decreases with population isolation and increases with local habitat suitability and stability since the Last Glacial Maximum (LGM). Second, we employed a recently developed multiple matrix regression with randomisation (MMRR) approach to study the factors associated with genetic divergence among the studied populations and test the relative contribution of environmental and geographic isolation to contemporary patterns of genetic differentiation. We found that genetic diversity was negatively correlated with average genetic differentiation with other populations, indicating that isolation and limited gene flow have contributed to erode genetic variability in some populations. Considering the relatively small size of the study area (<120 km), analyses of genetic structure indicate a remarkable inter‐population genetic differentiation. Environmental dissimilarity and differences in current and past climate niche suitability and their additive effects were not associated with genetic differentiation after controlling for geographic distance, indicating that local climate does not contribute to explain spatial patterns of genetic structure. Overall, our data indicate that geographic isolation, but not current or past climate, is the main factor determining contemporary patterns of genetic diversity and structure within the southernmost peripheral populations of this tropical oak.     

Morphologic variation in the cranium and mandible of the white-tailed deer (Odocoileus virginianus): A comparative study of geographical and four biological distances

Several biological distances based on cranial and mandibular variation among breeding groups of white-tailed deer were calculated and compared with geographic distances among the groups. Distances based on epigenetic variation among ten groups were calculated using 16 non-metric variants of the cranium and mandible. Penrose's size and shape distances and Mahalanobis' D² distance were calculated for 11 groups; the calculations were based on seven skeletal and seven dental metric variables of the mandible. The biological distances were correlated with geographic distance as follows: the epigenetic distance, 0.74; Penrose's shape distance, 0.71; Penrose's size distance, 0.45; and Mahalanobis' distance, 0.37. All correlations were significant at the 0.01 level. The epigenetic and Penrose shape correlations were significantly higher than the Mahalanobis correlation. Because of the conditions under which the breeding groups were selected, it was assumed that genetic affinites among the groups would be a function of geographic distance. The results suggest that the epigenetic distance and Penrose's shape distance reflect genetic affinities among groups better than do the Penrose size and Mahalanobis distances.     

Contrasting effects of landscape features on genetic structure in different geographic regions in the ornate dragon lizard,Ctenophorus ornatus

Habitat fragmentation can have profound effects on the distribution of genetic variation within and between populations. Previously, we showed that in the ornate dragon lizard, Ctenophorus ornatus, lizards residing on outcrops that are separated by cleared agricultural land are significantly more isolated and hold less genetic variation than lizards residing on neighbouring outcrops connected by undisturbed native vegetation. Here, we extend the fine‐scale study to examine the pattern of genetic variation and population structure across the species' range. Using a landscape genetics approach, we test whether land clearing for agricultural purposes has affected the population structure of the ornate dragon lizard. We found significant genetic differentiation between outcrop populations (F_ST = 0.12), as well as isolation by distance within each geographic region. In support of our previous study, land clearing was associated with higher genetic divergences between outcrops and lower genetic variation within outcrops, but only in the region that had been exposed to intense agriculture for the longest period of time. No other landscape features influenced population structure in any geographic region. These results show that the effects of landscape features can vary across species' ranges and suggest there may be a temporal lag in response to contemporary changes in land use. These findings therefore highlight the need for caution when assessing the impact of contemporary land use practices on genetic variation and population structure.     

Epigenetic effects on the mouse mandible: common features and discrepancies in remodeling due to muscular dystrophy and response to food consistency

Background  

In wild populations phenotypic differentiation of skeletal structures is influenced by many factors including epigenetic interactions and plastic response to environmental influences, possibly blurring the expression of genetic differences. In contrast, laboratory animals provide the opportunity to separate environmental from genetic effects. The mouse mandible is particularly prone to such plastic variations because bone remodeling occurs late in postnatal ontogeny, in interaction with muscular loading. In order to understand the impact of this process on mandible morphology, we investigated how change in the masticatory function affects the mandible shape, and its pattern of variation. Breeding laboratory mice on food of different consistencies mimicked a natural variation in feeding ecology, whereas mice affected by the murine analogue of the Duchenne muscular dystrophy provided a case of pathological modification of the mastication process.     

Geometric morphometrics of the mandible in the Iberian desman,Galemys pyrenaicus (Mammalia: Soricomorpha): Is there a significant variation in form during post-weaning life?

Geometric morphometrics was applied on the mandible of the Iberian desman, Galemys pyrenaicus, to determine for the first time possible sexual and post-weaning shape variation of this structure in a talpid species. Analyses were complemented by evaluating the effect of sex and age on size. The sample consisted of collection specimens from locations in the Cantabrian Mountains (northern Spain). Desmans were grouped into four relative age classes according to tooth wear. The shape of the internal side of the mandible was represented by 15 two-dimensional landmarks. Once young desmans leave the nest there is no significant variation in the form (size and shape) of the mandible. Thus, possible osseous changes and tooth abrasion derived from ageing do not produce obvious variation in mandible form. Mandible shape was significantly correlated with mandible size, resulting in a range of shapes that varies from a slender to a robust morphology. This variation was independent of geographic factors. Since the effect of non-heritable environmental influences on mandible size and shape was negligible, it can be considered that the mandible form of post-weaned desmans is the direct product of interactions between different developmental processes.     

Geographical and latitudinal variation in growth patterns and adult body size of Swedish moose (Alces alces)

We examined the geographical pattern in growth and adult body size among 14 populations of Swedish moose (Alces alces) using data from 4,294 moose (1.5 years old) killed during the hunting season in 1989–1992. In both sexes, adult body mass was significantly positively correlated with latitude. Moose in northern populations had a 15–20% larger adult body mass than moose in the south. Juvenile body mass was correlated with neither latitude nor adult body mass. Thus, variation in time (years) and rate of body growth after the juvenile stage were responsible for most of the variation in adult body mass among populations. Moose in northern populations grew for approximately 2 more years of life than southern moose. In contrast to adult body mass, skeletal size (measured as jawbone length) was not correlated with latitude, suggesting that variation in adult body mass was primarily due to differences in fat reserves. Discrimination between population characteristics, such as moose density, climate, and the amount of browse available to moose, showed climatic harshness to be the most important variable explaining geographical variation in body mass among populations. The results support the notion that in mammals body size increases with latitude in accordance with Bergmann's rule. We conclude that (1) variation in patterns of growth after the juvenile stage is the main cause of the latitudinal trend in adult body size in moose, and (2) climatic conditions are a more important factor than population density and availability of food in explaining geographical variation in growth patterns and adult body mass between populations of Swedish moose.     

Range-wide genetic differentiation of Eugenia dysenterica (Myrtaceae) populations in Brazilian Cerrado

The analysis of geographic patterns in genetic variation has been one of the most important current tools to understand ecological and evolutionary processes underlying population structure. However, inferring such processes from population data may be misleading if biased geographic samples are analyzed. Here we expand previous analyses of Eugenia dysenterica population structure in Brazilian Cerrado, analyzing a larger number of populations distributed throughout a broader geographic region covering most of species' range. We provide new estimates of genetic diversity and population structure based on SSR markers from both neutral and genic regions, using several cluster and ordination techniques. These analyzes reveal a continuous northwestern-southeastern gradient in population differentiation, and not two distinct clusters of populations as suggested in some previous studies. This more comprehensive analysis also reinforces that a simple process of stochastic differentiation do not explain the observed patterns. Moreover, we conclude that explanations for population differentiation may focus on why genetic diversity decreases toward southeastern populations and not necessarily on barriers and interruption of gene flow creating regional patterns of population differentiation.     

The Role of Geographical and Ecological Factors on Population Divergence of the Neotropical otter <Emphasis Type="Italic">Lontra longicaudis</Emphasis> (Carnivora,Mustelidae)

The geographic distribution of the populations of a species are influenced by the spatial structure of the ecosystems, the environmental factors and the presence of geographic barriers. The Neotropical otter, Lontra longicaudis, is widely distributed throughout the Americas, where a wide range of environmental conditions and geographical features could promote genetic and morphological variation on the three currently recognized subspecies. In this study, we combined phylogeographic, morphometric and environmental niche modelling analyses to examine whether: (1) genetic variation is associated with the presence of barriers to gene flow and/or hydrography; (2) genetic and morphologic variation are associated with environmental variation; and (3) the observed variation in L. longicaudis populations corresponds to the previously defined subspecies. We found strong phylogeographic structure between the northern (L. l. annectens) and the two-southern subspecies (L. l. longicaudis and L. l. enudris), and although shallower, we also detected genetic differentiation between the two South American subspecies. Such genetic differentiation corresponds to the hydrography and to the geographical barriers characteristic of the distributional area of the species. We found a correlation between the shape of the skull and mandible with the environmental variation through the distribution of the species, and we rejected the hypothesis of niche equivalency and similarity between the three identified genetic lineages, suggesting adaptations to different environmental conditions. Our results support that the variation in environmental conditions, in concert with geographical barriers to gene flow and hydrography, have led to population divergence of L. longicaudis along the Neotropics. These results have important taxonomic implications for the species and its conservation.     

Use of a natural hybrid zone for genomewide association mapping of craniofacial traits in the house mouse

The identification of the genes involved in morphological variation in nature is still a major challenge. Here, we explore a new approach: we combine 178 samples from a natural hybrid zone between two subspecies of the house mouse (Mus musculus domesticus and Mus musculus musculus), and high coverage of the genome (~ 145K SNPs) to identify loci underlying craniofacial shape variation. Due to the long history of recombination in the hybrid zone, high mapping resolution is anticipated. The combination of genomes from subspecies allows the mapping of both, variation within subspecies and inter‐subspecific differences, thereby increasing the overall amount of causal genetic variation that can be detected. Skull and mandible shape were measured using 3D landmarks and geometric morphometrics. Using principal component axes as phenotypes, and a linear mixed model accounting for genetic relatedness in the mapping populations, we identified nine genomic regions associated with skull shape and 10 with mandible shape. High mapping resolution (median size of significant regions = 148 kb) enabled identification of single or few candidate genes in most cases. Some of the genes act as regulators or modifiers of signalling pathways relevant for morphological development and bone formation, including several with known craniofacial phenotypes in mice and humans. The significant associations combined explain 13% and 7% of the skull and mandible shape variation, respectively. In addition, a positive correlation was found between chromosomal length and proportion of variation explained. Our results suggest a complex genetic architecture for shape traits and support a polygenic model.     

Population dynamics of the endangered plant, Phaedranassa tunguraguae, from the Tropical Andean hotspot

The Tropical Andes is a diversity hotspot for plants, but there is a scant knowledge about patterns of genetic variation within its constituent species. Phaedranassa tunguraguae is an IUCN endangered plant species endemic to a single valley in the Ecuadorian Andes. We estimate the levels of genetic differentiation across the geographic distribution of P. tunguraguae using 12 microsatellite loci. We discuss factors that might influence the genetic structure of this species. Genetic distance was used to evaluate relationship among populations and geographic patterns. Bayesian methods were used to investigate population structure, migration, evidence of recent bottlenecks, and time of divergence. The 7 populations form 2 genetic clusters. These clusters show highly significant differentiation between them, along with isolation by distance. Allele richness decreases from the most diverse westernmost population to the least diverse easternmost population. The species overall shows an excess of homozygotes, with highest levels of inbreeding in the easternmost population. We found evidence of recent bottleneck events. Migration rates were in general low but were higher between populations within each of the clusters. Time of divergence between populations was related to historical volcanic activity in the area. Based on our results, we propose 2 management units for P. tunguraguae.