A meta-analysis of the heritability of developmental stability

The existence of additive genetic variance in developmental stability has important implications for our understanding of morphological variation. The heritability of individual fluctuating asymmetry and other measures of developmental stability have frequently been estimated from parent-offspring regressions, sib analyses, or from selection experiments. Here we review by meta-analysis published estimates of the heritability of developmental stability, mainly the degree of individual fluctuating asymmetry in morphological characters. The overall mean effect size of heritabilities of individual fluctuating asymmetry was 0.19 from 34 studies of 17 species differing highly significantly from zero (P < 0.0001). The mean heritability for 14 species was 0.27. This indicates that there is a significant additive genetic component to developmental stability. Effect size was larger for selection experiments than for studies based on parent-offspring regression or sib analyses, implying that genetic estimates were unbiased by maternal or common environment effects. Additive genetic coefficients of variation for individual fluctuating asymmetry were considerably higher than those for character size per se. Developmental stability may be significantly heritable either because of strong directional selection, or fluctuating selection regimes which prevent populations from achieving a high degree of developmental stability to current environmental and genetic conditions.     

A study of wing morphology and fluctuating asymmetry in interspecific hybrids between Drosophila buzzatii and D. koepferae

In this work we investigate the effect of interspecific hybridization on wing morphology using geometric morphometrics in the cactophilic sibling species D. buzzatii and D. koepferae. Wing morphology in F₁ hybrids exhibited an important degree of phenotypic plasticity and differs significantly from both parental species. However, the pattern of morphological variation between hybrids and the parental strains varied between wing size and wing shape, across rearing media, sexes, and crosses, suggesting a complex genetic architecture underlying divergence in wing morphology. Even though there was significant fluctuating asymmetry for both, wing size and shape in F₁ hybrids and both parental species, there was no evidence of an increased degree of fluctuating asymmetry in hybrids as compared to parental species. These results are interpreted in terms of developmental stability as a function of a balance between levels of heterozygosity and the disruption of coadaptation as an indirect consequence of genomic divergence.     

FLUCTUATING ODONTOMETRIC ASYMMETRY,MORPHOLOGICAL VARIABILITY,AND GENETIC MONOMORPHISM IN THE CHEETAH ACINONYX JUBATUS

The magnitudes of dimensional variability and fluctuating asymmetry in dental dimensions are reported for a sample of South African cheetah Acinonyx jubatus. To test the hypothesis that elevated levels of variability and asymmetry are associated with the increased developmental instability reported for this species, our results were contrasted to those for two other felids: Felis lybica and F. caracal. These findings suggest that dental dimensions in cheetahs are not significantly more variable or asymmetric. Hence, it is concluded that the cheetah may not be as developmentally unstable as was previously supposed.     

Genetic homeostasis and developmental stability in natural populations of bisexual (<Emphasis Type="Italic">Carassius auratus</Emphasis>) and unisexual (<Emphasis Type="Italic">C. gibelio</Emphasis>) goldfishes

One amphymictic diploid Carassius auratus, three apomictic triploids C. gibbelio, and a hybrid triploid Carassius auratus forms of goldfish were compared with respect to a set of characteristics of developmental stability: morphological variation, fluctuating asymmetry, and phenodeviations. It was found that C. gibbelio forms are characterized by lower levels both of morphological variation and fluctuating symmetry and more rare morphological abnormalties. A hybrid form Carassius auratus-gibelio was characterized by the intermediate values of the above-listed features. It is emphasized that phenotypic stabilization of apomictic forms is caused by two factors: its clone structure and actual developmental canalization. It is specified that promoted genetic homeostasis of the C. gibelio form does not give obvious adaptive advantages, as in the basic river basins of East and Central Europe. they are everywhere ousted by an amphimictic C. auratus.     

Phylogeography, genetic structure and population divergence time of cheetahs in Africa and Asia: evidence for long-term geographic isolates

The cheetah (Acinonyx jubatus) has been described as a species with low levels of genetic variation. This has been suggested to be the consequence of a demographic bottleneck 10 000–12 000 years ago (ya) and also led to the assumption that only small genetic differences exist between the described subspecies. However, analysing mitochondrial DNA and microsatellites in cheetah samples from most of the historic range of the species we found relatively deep phylogeographic breaks between some of the investigated populations, and most of the methods assessed divergence time estimates predating the postulated bottleneck. Mitochondrial DNA monophyly and overall levels of genetic differentiation support the distinctiveness of Northern‐East African cheetahs (Acinonyx jubatus soemmeringii). Moreover, combining archaeozoological and contemporary samples, we show that Asiatic cheetahs (Acinonyx jubatus venaticus) are unambiguously separated from African subspecies. Divergence time estimates from mitochondrial and nuclear data place the split between Asiatic and Southern African cheetahs (Acinonyx jubatus jubatus) at 32 000–67 000 ya using an average mammalian microsatellite mutation rate and at 4700–44 000 ya employing human microsatellite mutation rates. Cheetahs are vulnerable to extinction globally and critically endangered in their Asiatic range, where the last 70–110 individuals survive only in Iran. We demonstrate that these extant Iranian cheetahs are an autochthonous monophyletic population and the last representatives of the Asiatic subspecies A. j. venaticus. We advocate that conservation strategies should consider the uncovered independent evolutionary histories of Asiatic and African cheetahs, as well as among some African subspecies. This would facilitate the dual conservation priorities of maintaining locally adapted ecotypes and genetic diversity.     

Extremely Low Levels of Allozyme Variation in Southern Korean Populations of the Two Rare and Endangered Lithophytic or Epiphytic <Emphasis Type="Italic">Bulbophyllum Drymoglossum</Emphasis> and <Emphasis Type="Italic">Sarcanthus Scolopendrifolius</Emphasis> (Orchidaceae): Implications for Conservation

Allozyme variation was investigated in two local populations of Bulbophyllum drymoglossum and three populations Sarcanthus scolopendrifolius, two rare and endangered lithophytes and epiphytes from South Korea. Genetic diversity was extremely low within populations (mean H _e = 0.011 for B. drymoglossum; 0.002 for S. scolopendrifolius). Among the putative screened 21 loci, we found only one polymorphic locus for each species. Only one polymorphic locus, detected just one population of each species, revealed significantly high degree of population differentiation between and among populations (F _ST = 0.253 for B. drymoglossum and F _ST = 0.899 for S. scolopendrifolius). These results suggest that genetic drift (consequence of a very small effective population size), coupled with a limited gene flow would play a major role in shaping population genetics of these species in South Korea. The current status of both species (small population sizes, spatially isolated populations, and highly localized habitats) in addition to the extremely low levels of genetic diversity and reckless collection of endangered orchids by plant sellers, significantly threaten the long-term survival of these species in Korea. Conservation of the two species requires both in situ strategies, by introducing of genets to increase effective population sizes by minimizing adverse effects (e.g., outbreeding depression and genetic swamping by non-native genotypes), and ex situ strategies, such as collection of genets from clonal ramets.     

GENETIC VARIATION IN ALETES ACAULIS AND ITS RELATIVE,THE NARROW ENDEMIC A. HUMILIS (APIACEAE)

We compared the organization of genetic variability in Aletes humilis, a species restricted to seven populations in north-central Colorado, with A. acaulis, a closely related widespread species. Genetic variability was scored at 11 electrophoretically detectable protein loci. Nine of these loci were polymorphic (i.e., P > 0.95) in both taxa, and were used for interpopulation and interspecific comparisons. Levels of genetic variability and patterns of organization of this variability are very comparable in both species. In contrast to many other narrow endemics, A. humilis is not genetically depauperate when compared to its presumed progenitor. Both biochemical and morphological evidence suggest that A. humilis is derived from A. acaulis; the comparable levels of variability in the two species suggest that A. humilis was derived from a source containing a substantial portion of the original A. acaulis genome, because there is no evidence of a genetic bottleneck or appreciable loss of allelic variability.     

Genetic and morphological variation in two littorinid gastropods: evidence for recent population expansions along the East African coast

In marine species, population diversity and differentiation is affected by the population history and by the complex interaction between oceanographic dynamics and ecological traits. In the present study, we examined two species of marine gastropods (the mangrove periwinkle Littoraria scabra and the rocky shore Littoraria glabrata) along the East African coast, using both genetic and geometric morphometric methods. We report a greater variation of shell shape in L. scabra compared to the slightly smaller variation in L. glabrata. This variation was probably associated with variation of environmental factors along the coast, such as temperature and hydrodynamics. Despite morphological variation, we found low mitochondrial genetic differentiation among samples from different localities for both species, which is probably a consequence of the ongoing gene flow during the free‐swimming larval stage of these gastropods. Additionally, high levels of haplotype diversity, low nucleotide diversity, and ‘star‐like’ genealogies were found in both species. These observations and the results from mismatch distributions, indicate a possible signature of recent population expansions in both species, which probably started during interglacial periods of the Pleistocene and led to the colonization of the Indian Ocean coast. © 2013 The Linnean Society of London     

Habitat fragmentation promotes fluctuating asymmetry but not morphological divergence in two geckos

The process of species formation is often ignored in discussions on the conservation of biodiversity. Yet the clearance of vegetation may promote divergence among populations of a species through isolation, providing conditions for rapid genetic drift and novel selection pressures. Here, stepwise discriminant function analysis and fluctuating asymmetry are used to examine variation in morphology within and among non fragmented and recently fragmented populations of two species of gecko,Oedura reticulata andGehyra variegata. High reclassification error rates using discriminant function analysis, indicate that fragmentation has had no detectable effect on morphological differentiation among populations of either species. In contrast, remnant populations of both species exhibit higher mean levels of fluctuating asymmetry than do populations in undisturbed habitat. ForOedura reticulata, levels of fluctuating asymmetry are negatively correlated with the log of adult population size. These results suggest that the changes following habitat clearance have been severe enough to cause increased developmental instability in populations of both species but not detectable morphological divergence. Given the high rate of extirpation of gecko populations in the study region and the extreme vulnerability of the remaining populations, it is unlikely that species formation will be significant in maintaining reptile diversity in that region.     

Cryptic or pseudocryptic: can morphological methods inform copepod taxonomy? An analysis of publications and a case study of the Eurytemora affinis species complex

Interest in cryptic species has increased significantly with current progress in genetic methods. The large number of cryptic species suggests that the resolution of traditional morphological techniques may be insufficient for taxonomical research. However, some species now considered to be cryptic may, in fact, be designated pseudocryptic after close morphological examination. Thus the “cryptic or pseudocryptic” dilemma speaks to the resolution of morphological analysis and its utility for identifying species. We address this dilemma first by systematically reviewing data published from 1980 to 2013 on cryptic species of Copepoda and then by performing an in‐depth morphological study of the former Eurytemora affinis complex of cryptic species. Analyzing the published data showed that, in 5 of 24 revisions eligible for systematic review, cryptic species assignment was based solely on the genetic variation of forms without detailed morphological analysis to confirm the assignment. Therefore, some newly described cryptic species might be designated pseudocryptic under more detailed morphological analysis as happened with Eurytemora affinis complex. Recent genetic analyses of the complex found high levels of heterogeneity without morphological differences; it is argued to be cryptic. However, next detailed morphological analyses allowed to describe a number of valid species. Our study, using deep statistical analyses usually not applied for new species describing, of this species complex confirmed considerable differences between former cryptic species. In particular, fluctuating asymmetry (FA), the random variation of left and right structures, was significantly different between forms and provided independent information about their status. Our work showed that multivariate statistical approaches, such as principal component analysis, can be powerful techniques for the morphological discrimination of cryptic taxons. Despite increasing cryptic species designations, morphological techniques have great potential in determining copepod taxonomy.     

Analysis of asymmetries in the African fruit bats Eidolon helvum and Rousettus egyptiacus (Mammalia: Megachiroptera) from the islands of the Gulf of Guinea. II. Integration and levels of multivariate fluctuating asymmetry across a geographical range

Using a set of cranial morphometric characters, trends of variation in multivariate fluctuating asymmetry were evaluated and compared in populations of African fruit bats Rousettus egyptiacus and Eidolon helvum from the Gulf of Guinea islands, and the adjacent mainland. Levels of asymmetry were compared across populations and species, and significant differences were found in both comparisons. Differences coincided with species‐specific patterns of morphological and genetic differentiation. Concordance of correlation matrices of asymmetry was also compared. Results were significant; concordance is hypothesized to be a by‐product of developmental processes that produce the ‘fox‐like’ morphology shared by these species. Consistency of asymmetry patterns suggests that the developmental pathway producing it is highly canalized. A prediction of the above hypothesis is that a radical change in the ‘fox‐like’ structural pattern would result in breakage of the asymmetry parameter associated with it.     

Surprising diversity in the Pannonian populations of Marsh Fritillary (Euphydryas aurinia,Lepidoptera: Nymphalidae): Morphometric and molecular aspects

Since genetic variation is the basis of evolutionary potential of a species, its structure needs to be understood. Thus, the aim of this study was to analyze and contrast the structure of genetic and phenotypic variation in the Euphydryas aurinia populations of southeastern central Europe. Genetic variation was studied by two types of molecular genetic markers: mtDNA COI sequences and allozymes. As the great hiatus in the European distribution of E. aurinia is located in the central part of the Carpathian Basin, we expected that the populations East and West to this gap would be highly differentiated. Populations of Central Transdanubia actually represent the easternmost margin of the West European distribution of E. aurinia. In view of the peripheral position of these populations, we supposed to find some genetic sign of local adaptation, as a consequence of diversifying selection and an increased level of fluctuating asymmetry as a result of environmental stress. The analyses of the molecular genetic markers revealed a basic East–West differentiation among the populations of southeastern central Europe which was further structured in the western part of the study area. The results suggested that the genetic differentiation between the two western regions is probably the consequence of diversifying selection. The pattern of phenotypic differentiation among the western populations, however, was different. A geographic cline was revealed (decreasing wing size) toward the eastern margin of the distribution in parallel with increasing fluctuating asymmetry. The conservation inferences of the results are considered.     

GEOMETRIC MORPHOMETRICS OF DEVELOPMENTAL INSTABILITY: ANALYZING PATTERNS OF FLUCTUATING ASYMMETRY WITH PROCRUSTES METHODS

Although fluctuating asymmetry has become popular as a measure of developmental instability, few studies have examined its developmental basis. We propose an approach to investigate the role of development for morphological asymmetry by means of morphometric methods. Our approach combines geometric morphometrics with the two-way ANOVA customary for conventional analyses of fluctuating asymmetry and can discover localized features of shape variation by examining the patterns of covariance among landmarks. This approach extends the notion of form used in studies of fluctuating asymmetry from collections of distances between morphological landmarks to an explicitly geometric concept of shape characterized by the configuration of landmarks. We demonstrate this approach with a study of asymmetry in the wings of tsetse flies (Glossina palpalis gambiensis). The analysis revealed significant fluctuating and directional asymmetry for shape as well as ample shape variation among individuals and between the offspring of young and old females. The morphological landmarks differed markedly in their degree of variability but multivariate patterns of landmark covariation identified by principal component analysis were generally similar between fluctuating asymmetry (within-individual variability) and variation among individuals. Therefore there is no evidence that special developmental processes control fluctuating asymmetry. We relate some of the morphometric patterns to processes known to be involved in the development of fly wings.     

Intra- and interspecific allozymic variation in Liparis fabricii and Liparis gibbus (Teleostei,Liparididae) from Spitsbergen waters

Summary In the literature, arctic snailfish of the genus Liparis are often identified as L. liparis, primarily due to the wide morphological variation reported for this species. Recent morphological studies have, however, identified separate arctic Liparis species. Electrophoretic studies of the genetic relationship between two such species (L. fabricii and L. gibbus), from deepwater localities west of Spitsbergen revealed significant differences in allozyme mobility at a series of gene-loci and thus supported the evidence that they are valid species. Their extremely low intra-specific variability, with average heterozygosities well below one percent, is comparable to measures for other polar teleosts. No protein coding locus was found suitable for studies of possible population structuring of L. gibbus due to the very low frequencies of all but the commonest allele.     

Estimating genetic and phenotypic diversity in a northern hoverfly reveals lack of heterozygosity correlated with significant fluctuating asymmetry of wing traits

The genetic structure and phenotypic diversity of a population of Cheilosia naruska Haarto and Kerppola, 2007 (Diptera, Syrphidae) from Lapland, Finland, was examined through allozyme electrophoresis and wing morphometrics. The morphological identification of the species was verified molecularly using partial sequences of mitochondrial COI and the nuclear ribosomal ITS2 genes comparing with corresponding sequences of a paratype of the taxon. Based on protein electrophoresis, out of 12 analyzed allozyme loci, only one locus (Me) was found to be polymorphic. The low genetic variability was further evidenced by the absence of heterozygote genotypes. Fluctuating asymmetry was used as a measure of developmental stability. For this we used different wing traits that were estimated using both wing landmark positions and metric traits. Procrustes ANOVA and Canonical variate analysis revealed asymmetry in wing metric and wing shape and size, and within each sex considered separately. Principal component analysis revealed similar multivariate patterns of landmark covariation between within-individual variability (fluctuating asymmetry) and variation among individuals. Finally, the observed association between lack of heterozygosity and high level of asymmetry is discussed in light of conservation.     

POPULATION STRUCTURE AND ESTIMATES OF GENE FLOW IN THE HOMOSPOROUS FERN POLYSTICHUM MUNITUM

Levels and distribution of genetic variation were investigated in the homosporous fern, Polystichum munitum. Homosporous ferns differ from higher vascular plants in that they possess potentially bisexual gametophytes which can produce a completely homozygous sporophyte in a single generation. Because of this, it has long been maintained that ferns possess an inbreeding mating system, resulting in low levels of genetic variation and high levels of homozygosity within populations. The four populations sampled maintain high levels of genetic variation (P? = 0.542; H? = 0.111; ā = 2.23), comparable to that maintained by populations of outcrossing seed plants. The mean fixation index, F, for the four populations was 0.052, indicating no significant deviations from Hardy-Weinberg genotypic expectations. Polystichum munitum distributes most of its genetic variation within rather than among populations. Population-genetic structure was assessed by subdividing each of two large populations into 10 × 10-m subpopulations. Comparisons of genetic variation within and among subpopulations indicated little genetic substructure within either of the artificially subdivided populations. Estimates of interpopulational gene flow (Nm) are extremely high, comparable to those reported for gymnosperms. Statistical estimates of intragametophytic selling are very low, ranging from 0 to 3%. This study suggests that Polystichum munitum is an outcrossing species. Evidence from this and other investigations indicates that fern species do not typically self-fertilize and that mating systems in ferns vary as they do among species of seed plants.     

Allozyme variation and population differentiation of the Aconitum delavayi complex (Ranunculaceae) in the Hengduan Mountains of China

The Aconitum delavayi complex is a group of four climbing species with trisect-leaves occurring in the Hengduan Mountains. The species of this complex are highly localized on very narrow regions with quite small population sizes. Because of rapid environmental changes recently in the Hengduan Mountains, this complex shows complicated morphological variability, which makes it difficult to delimit species. In the present study, 10 enzyme systems coding for 14 putative loci were employed to detect the interspecific and intraspecific genetic variation of the complex. In addition to low genetic diversity within all eight populations surveyed, the results indicate that A. episcopale is a distinct species because of high genetic identities among its three populations. Very low genetic divergence among populations of A. stapfianum and A. delavayi suggests that the two species should be treated as a single one.     

Genetic Evidence of the Contribution of Ethnic Migrations to the Propagation and Persistence of the Rare and Declining Scrambling Shrub Caesalpinia bonduc L

This paper examines the contribution of human migrations to the propagation and maintenance of Caesalpina bonduc by means of an analysis of its population genetics and distribution patterns. One hundred and forty seven sites were surveyed in the three climatic zones of Benin and all individuals of the species were recorded. A set of individuals was randomly selected and sampled from seven populations and morphological variation and genetic diversity were assessed. The study confirmed the presence of the species in all climatic zones but its abundance varied greatly. Morphological variability between populations and zones was low in comparison with the high amount of variation within populations. AFLP and cpDNA fingerprinting revealed an extremely low genetic diversity within populations and a low genetic differentiation, suggesting parental links between populations. The results support the hypothesis of human involvement in Caesalpinia dispersal and persistence in Benin. However, the low genetic diversity may imply high risks for future extinction. We recommend that gene flow among the remaining populations be supported in order to conserve the species.     

Regional variation in the cheetah (Acinonyx jubatus) revisited: Morphology of wild and captive populations

The cheetah (Acinonyx jubatus) is listed as a vulnerable species by the International union for the conservation of nature (IUCN), including two critically endangered subspecies, the Saharan cheetah, and the Iranian cheetah, so it is imperative that we understand variation in cheetah morphology to make good decisions regarding the conservation of this species. Here, we aim to determine whether northeastern African cheetahs have smaller body sizes than southern African cheetahs. This study also adds to our knowledge of cheetah morphology from two cheetah populations that do not yet have comprehensive published data: Kenya, and northeastern Africa, including captive individuals. We calculated means and standard deviations on cranial and body measurements of live or in few cases, freshly dead, cheetahs from the aforementioned populations, plus previously published data on Namibian and Botswanan cheetahs and compared them to one another using multivariate analysis of variance. Results show that northeastern African cheetahs have smaller body sizes than southern and eastern African populations. We also found that captive cheetahs retain the morphological characteristics of their ancestral population- captive cheetahs from southern Africa have similar body sizes to wild southern African cheetahs and larger body sizes than captives from northeastern Africa. Other analyses regarding cheetah growth agree with previous studies on Namibian and Botswanan cheetah populations rates. As such, this study can serve as a baseline for the care of captive cheetah populations to maintain healthy weights and body proportions.