Patterns Of Phenotypic Variation Research Articles

Geographically multifarious phenotypic divergence during speciation

Speciation is an important evolutionary process that occurs when barriers to gene flow evolve between previously panmictic populations. Although individual barriers to gene flow have been studied extensively, we know relatively little regarding the number of barriers that isolate species or whether these barriers are polymorphic within species. Herein, we use a series of field and lab experiments to quantify phenotypic divergence and identify possible barriers to gene flow between the butterfly species Lycaeides idas and Lycaeides melissa. We found evidence that L. idas and L. melissa have diverged along multiple phenotypic axes. Specifically, we identified major phenotypic differences in female oviposition preference and diapause initiation, and more moderate divergence in mate preference. Multiple phenotypic differences might operate as barriers to gene flow, as shown by correlations between genetic distance and phenotypic divergence and patterns of phenotypic variation in admixed Lycaeides populations. Although some of these traits differed primarily between species (e.g., diapause initiation), several traits also varied among conspecific populations (e.g., male mate preference and oviposition preference).

Phenotypic characters of rice landraces reveal independent lineages of short-grain aromatic indica rice.

Rice landraces are lineages developed by farmers through artificial selection during the long-term domestication process. Despite huge potential for crop improvement, they are largely understudied in India. Here, we analyse a suite of phenotypic characters from large numbers of Indian landraces comprised of both aromatic and non-aromatic varieties. Our primary aim was to investigate the major determinants of diversity, the strength of segregation among aromatic and non-aromatic landraces as well as that within aromatic landraces. Using principal component analysis, we found that grain length, width and weight, panicle weight and leaf length have the most substantial contribution. Discriminant analysis can effectively distinguish the majority of aromatic from non-aromatic landraces. More interestingly, within aromatic landraces long-grain traditional Basmati and short-grain non-Basmati aromatics remain morphologically well differentiated. The present research emphasizes the general patterns of phenotypic diversity and finds out the most important characters. It also confirms the existence of very unique short-grain aromatic landraces, perhaps carrying signatures of independent origin of an additional aroma quantitative trait locus in the indica group, unlike introgression of specific alleles of the BADH2 gene from the japonica group as in Basmati. We presume that this parallel origin and evolution of aroma in short-grain indica landraces are linked to the long history of rice domestication that involved inheritance of several traits from Oryza nivara, in addition to O. rufipogon. We conclude with a note that the insights from the phenotypic analysis essentially comprise the first part, which will likely be validated with subsequent molecular analysis.

Inter-island but not intra-island divergence among populations of sea oats, Uniola paniculata L. (Poaceae)

Understanding the underlying causes of phenotypic trait variation among populations is important for informing conservation decisions. This knowledge can be used to determine whether locality matters when sourcing populations for habitat restoration. Uniola paniculata is a federally protected coastal dune grass native to the southeastern Atlantic and the Gulf coasts of the USA that is often used to stabilize restored dune habitats. This study uses neutral genetic markers (allozymes) and a greenhouse common garden study to determine the relative contributions of neutral evolutionary processes and natural selection to patterns of phenotypic variation among natural populations of U. paniculata. Seeds were sourced from foredune and backdune populations spanning shoreline-to-landward environmental gradients on each of four Georgia barrier islands. Based on previous work, we expected to find evidence of divergent selection among populations located on the shoreline-to-landward environmental gradient. However, differences among islands, rather than intra-island habitat differences, drive divergent selection on aboveground and total biomass. The lack of evidence for divergent selection across the shoreline-to-landward gradient suggests that previously documented intra-island trait variation is likely due to phenotypic plasticity. Our findings have implications for conservation and restoration efforts involving U. paniculata, as there is evidence for divergent selection among populations located on neighboring islands.

Pathogen Diversity and Hidden Regimes of Apparent Competition

Competition through cross-reacting host immune responses, a form of apparent competition, is a major driver of pathogen evolution and diversity. Most models of pathogens have focused on intraspecific interactions to explain observed patterns. Two recent experiments suggested that Haemophilus influenzae, a common nasopharyngeal colonizer of humans, might alter the immune environment in a way that favors otherwise less fit serotypes of another common pathogen, pneumococcus. Using a computational model, we demonstrate that H. influenzae, if it consistently raises the fitness of the less fit serotypes, can strongly promote pneumococcal diversity. However, the effects of H. influenzae are so sensitive to the prevalence of H. influenzae that this species is unlikely to be the main driver of serotype coexistence. Interactions that significantly affect diversity could furthermore be extremely difficult to detect through co-occurrence analysis alone. These results suggest that small differences in strains' adaptations to different immunological regimes, which are shaped by coinfections with other pathogens, can have dramatic effects on strain dynamics and patterns of phenotypic variation. Studies of microbial communities might therefore benefit from the use of varied approaches to infer the presence of indirect interactions.

A Forest Butterfly in Sahara Desert Oases: Isolation Does Not Matter

Numerous studies addressing the impact of habitat fragmentation on genetic diversity have been performed. In this study, we analyze the effects of a seemingly nonpermeable matrix on the population structure of the forest-dwelling butterfly Pararge aegeria in geographically isolated oases at the northern margin of the Sahara desert using microsatellites, morphological characters, and species distribution modeling. Results from all analyses are mostly congruent and reveal 1) a split between European and North African populations, 2) rather low divergence between populations from the eastern and western part of North Africa (Morocco vs. Tunisia), 3) a lack of differentiation between the oasis and Atlas Mountain populations, 4) as well as among the oasis populations, and 5) no reduction of genetic variability in oasis populations. However, one exception to this general trend resulted from the analyses of wing shape; wings of butterflies from oases are more elongated compared with those from the other habitats. This pattern of phenotypic divergence may suggest a recent colonization of the oasis habitats by individuals, which might be accompanied by a rather dispersive behavior. Species distribution modeling suggests a fairly recent reexpansion of the species' climatic niche starting in the Holocene at about 6000 before present. The combined results indicate a rather recent colonization of the oases by highly mobile individuals from genetically diverse founder populations. The colonization was likely followed by the expansion and persistence of these founder populations under relatively stable environmental conditions. This, together with low rates of gene flow, likely prevented differentiation of populations via drift and led to the maintenance of high genetic diversity.

Seedling development in a Brassica napus diversity set and its relationship to agronomic performance

Brassica napus L. is the leading European oilseed crop and has therefore a high economical importance. The objectives of our study were to examine (1) the patterns of phenotypic diversity in a species-wide B. napus germplasm set of 518 inbreds with respect to various seedling development, agronomic, and seed quality traits as well as (2) the interrelationship of the examined traits and their use in selection on correlated traits. The B. napus germplasm set was evaluated in greenhouse and field trials for several seedling development, agronomic, and seed quality traits. The traits were highly correlated within the individual trait categories and moderately correlated between the different trait categories. We observed differences in phenotypic diversity among the examined eight germplasm types. The reduction of phenotypic diversity was on average more pronounced for the seedling development traits than for the agronomic and seed quality traits, suggesting that plant breeders need to introgress new genetic variation with respect to the former.

Limb Abnormalities in Two Species ofLerista(Scincidae, Squamata)

This article presents a survey of phenotypic variation in the limbs of two species of Lerista, a diverse clade of Australian scincid lizards widely considered to provide the best available model for studying squamate limb reduction and loss. Abnormalities were observed in 4.1% of forelimbs and 5.4% of hind limbs in the tetradactyl species L. dorsalis, and 4.5% of forelimbs and 2.4% of hind limbs in the tridactyl species L. timida. Substantial malformation of the manus or pes, involving the complete absence or severe reduction of all digits, accounts for a considerable proportion of anomalies in both species. Almost all remaining anomalies involve the absence or severe reduction of one or two digits. Despite the moderate frequency of limb abnormalities recorded, no cases of supernumerary digits were observed. Patterns of phenotypic variation in both species are consistent with the conventional perspective that substantial limb reduction is effectively irreversible, and provide support for the conclusion that structurally reduced limbs have not been re-elaborated in Lerista.

Patterns of Ancestry, Signatures of Natural Selection, and Genetic Association with Stature in Western African Pygmies

African Pygmy groups show a distinctive pattern of phenotypic variation, including short stature, which is thought to reflect past adaptation to a tropical environment. Here, we analyze Illumina 1M SNP array data in three Western Pygmy populations from Cameroon and three neighboring Bantu-speaking agricultural populations with whom they have admixed. We infer genome-wide ancestry, scan for signals of positive selection, and perform targeted genetic association with measured height variation. We identify multiple regions throughout the genome that may have played a role in adaptive evolution, many of which contain loci with roles in growth hormone, insulin, and insulin-like growth factor signaling pathways, as well as immunity and neuroendocrine signaling involved in reproduction and metabolism. The most striking results are found on chromosome 3, which harbors a cluster of selection and association signals between approximately 45 and 60 Mb. This region also includes the positional candidate genes DOCK3, which is known to be associated with height variation in Europeans, and CISH, a negative regulator of cytokine signaling known to inhibit growth hormone-stimulated STAT5 signaling. Finally, pathway analysis for genes near the strongest signals of association with height indicates enrichment for loci involved in insulin and insulin-like growth factor signaling.

Fine-scale local adaptation in life histories along a continuous environmental gradient in Trinidadian guppies

Summary 1. Theoretical models of life-history evolution predict a continuum of fast to slow life histories, yet most of empirical support for this theory comes from studies that have considered dichotomous environments (i.e. high vs. low food, presence or absence of major predators). Although this approach has been very successful in identifying the signature of local adaptation, it might limit our ability to identify the causes of underlying patterns of phenotypic variation. By studying the variation in life-history traits along continuous gradients, we can gain better insight into the diversity of adaptations exhibited by natural populations. 2. We studied the evolution of life-history traits along a gradient of predation pressure in the Trinidadian guppy (Poecilia reticulata). Six localities along the Guanapo–Caroni River drainage were selected with respect to their predator community, going from upstream localities where guppies only coexist with a single gape-limited fish predator, to lowland sites where guppies coexist with a complex fish community. Along this gradient, we characterized the field pattern of phenotypic variation in age and size at maturity and reproductive effort. Further, to determine the genetic basis of this variation, we measured these traits in second-generation laboratory-born fish from the same localities sampled in the wild. 3. In nature, we found a fine-scale pattern of phenotypic variation in most life-history traits that paralleled the continuous predation gradient. In the laboratory, we observed that reproductive allocation and brood size progressively decrease while age at maturity and interbrood interval progressively increase with a reduction in the predator community, suggesting a genetic basis to the parallel patterns observed in the field for reproductive allocation and offspring number. 4. However, there were some exceptions to the observed pattern of variation. Females from one low-predation locality matured younger and reproduced more frequently than expected based upon the simple nature of the fish community. We also found significant differences between our field and laboratory results for embryo size, suggesting that this trait is highly plastic. 5. Our results imply that local adaptation in guppies occurs at a finer scale than has previously been shown. Furthermore, while our results are consistent with predator-driven life-history variation, we also find patterns of plasticity that would not be apparent in the traditional dichotomous approach.

Geographic patterns and environmental drivers of flower and leaf variation in an endemic legume of Southern Patagonia

Background: In widely distributed species, geographic patterns of phenotypic variation can appear in a clinal (linear or central–marginal) or mosaic fashion in response to environmental factors. Aim: We assessed spatial patterns and possible abiotic drivers of flower and leaf variation in Anarthrophyllum desideratum, an endemic legume found throughout a wide environmental gradient in southern Patagonia. Methods: We measured 10 floral and foliar traits from 26 populations, distributed along the entire range of the species. We examined phenotypic variation within and among populations, geographical patterns, relationships with climatic and edaphic factors and spatial covariation between flowers and leaves, using uni- and multivariate analyses. Results: Most of the studied traits showed higher variability among than within populations. Within-population variability was not associated with population size. Phenotypic differences among populations were structured by geographic distances. Clinal variation patterns, mainly central–marginal, were detected along a south-west to north-east gradient. Flower and leaf size co-varied across populations, whereas, overall phenotypes were weakly coupled. Phenotypic variation was associated with temperature and soil potassium content. Conclusions: Our results support geographically structured patterns of phenotypic variation and suggest that the abiotic environment has an important role in shaping floral and foliar differences among A. desideratum populations. Non-stochastic processes may account for the geographical variation found in this species.

Contemporary and historical evolutionary processes interact to shape patterns of within‐lake phenotypic divergences in polyphenic pumpkinseed sunfish, Lepomis gibbosus

Historical and contemporary evolutionary processes can both contribute to patterns of phenotypic variation among populations of a species. Recent studies are revealing how interactions between historical and contemporary processes better explain observed patterns of phenotypic divergence than either process alone. Here, we investigate the roles of evolutionary history and adaptation to current environmental conditions in structuring phenotypic variation among polyphenic populations of sunfish inhabiting 12 postglacial lakes in eastern North America. The pumpkinseed sunfish polyphenism includes sympatric ecomorphs specialized for littoral or pelagic lake habitats. First, we use population genetic methods to test the evolutionary independence of within-lake phenotypic divergences of ecomorphs and to describe patterns of genetic structure among lake populations that clustered into three geographical groupings. We then used multivariate analysis of covariance (MANCOVA) to partition body shape variation (quantified with geometric morphometrics) among the effects of evolutionary history (reflecting phenotypic variation among genetic clusters), the shared phenotypic response of all populations to alternate habitats within lakes (reflecting adaptation to contemporary conditions), and unique phenotypic responses to habitats within lakes nested within genetic clusters. All effects had a significant influence on body form, but the effects of history and the interaction between history and contemporary habitat were larger than contemporary processes in structuring phenotypic variation. This highlights how divergence can be better understood against a known backdrop of evolutionary history.

Are phenotypic traits useful for differentiating among a priori Coregonus taxa?

A key for three putative species apparently found in three geographic areas, i.e. Coregonus clupeoides (in Scotland), Coregonus stigmaticus (in England), and Coregonus pennantii (in Wales) given in a recent review was tested quantitatively using 544 individuals from nine populations. The classification success of the key was very low (27%). It was concluded that there is currently no robust evidence for the recognition of the three putative species. Furthermore, the use of phenotypic characters alone to distinguish putative species in postglacial fish species such as those of the genus Coregonus that show homoplasy in many of these traits is questioned. In the absence of further evidence, it was concluded that a single highly variable species best describes the pattern of phenotypic variation in these U.K. populations. On this basis it is argued that taxonomic subdivision of U.K. European coregonids is inappropriate and that Coregonus lavaretus should prevail as the species name applicable to all populations.

Patterns of phenotypic variation reveal substantial differentiation in sexual dimorphism of three Psammodromus (Squamata, Lacertidae) species

The Spanish sand racer (Psammodromus hispanicus) has been recently split into three distinct species: P. hispanicus, P. edwardsianus, and P. occidentalis. Some morphological differences have been reported but there is as yet no description allowing unambiguous identification of the three species. Here, we describe differentiation in body measurements, scalation traits, and colour traits as well as in the degree of sexual dimorphism. Our results show that P. edwardsianus can be easily distinguished by the presence of a supralabial scale below the subocular scale, which is absent in the other two species. Psammodromus hispanicus and P. occidentalis can be distinguished by the number of femoral pores, throat scales and ocelli, and the relative width of the anal scale. The degree of sexual size dimorphism and sexual colour dimorphism substantially differs among species, suggesting that different scenarios of sexual and natural selection may exist for each species. Moreover, sexually selected traits (nuptial colouration, ocelli, and femoral pores) significantly differ among species, suggesting that visual and chemical communication may also differ among species. Such differences could prevent reproduction and gene flow at secondary contact zones, potentially reinforcing isolation and speciation within this group of lizards.

Regulatory versus coding signatures of natural selection in a candidate gene involved in the adaptive divergence of whitefish species pairs (Coregonus spp.)

While gene expression divergence is known to be involved in adaptive phenotypic divergence and speciation, the relative importance of regulatory and structural evolution of genes is poorly understood. A recent next-generation sequencing experiment allowed identifying candidate genes potentially involved in the ongoing speciation of sympatric dwarf and normal lake whitefish (Coregonus clupeaformis), such as cytosolic malate dehydrogenase (MDH1), which showed both significant expression and sequence divergence. The main goal of this study was to investigate into more details the signatures of natural selection in the regulatory and coding sequences of MDH1 in lake whitefish and test for parallelism of these signatures with other coregonine species. Sequencing of the two regions in 118 fish from four sympatric pairs of whitefish and two cisco species revealed a total of 35 single nucleotide polymorphisms (SNPs), with more genetic diversity in European compared to North American coregonine species. While the coding region was found to be under purifying selection, an SNP in the proximal promoter exhibited significant allele frequency divergence in a parallel manner among independent sympatric pairs of North American lake whitefish and European whitefish (C. lavaretus). According to transcription factor binding simulation for 22 regulatory haplotypes of MDH1, putative binding profiles were fairly conserved among species, except for the region around this SNP. Moreover, we found evidence for the role of this SNP in the regulation of MDH1 expression level. Overall, these results provide further evidence for the role of natural selection in gene regulation evolution among whitefish species pairs and suggest its possible link with patterns of phenotypic diversity observed in coregonine species.

The onion model, a simple neutral model for the evolution of diversity in bacterial biofilms

Bacterial biofilms are particularly resistant to a wide variety of antimicrobial compounds. Their persistence in the face of antibiotic therapies causes significant problems in the treatment of infectious diseases. Seldom have evolutionary processes like genetic drift and mutation been invoked to explain how resistance to antibiotics emerges in biofilms, and we lack a simple and tractable model for the genetic and phenotypic diversification that occurs in bacterial biofilms. Here, we introduce the 'onion model', a simple neutral evolutionary model for phenotypic diversification in biofilms. We explore its properties and show that the model produces patterns of diversity that are qualitatively similar to observed patterns of phenotypic diversity in biofilms. We suggest that models like our onion model, which explicitly invoke evolutionary process, are key to understanding biofilm resistance to bactericidal and bacteriostatic agents. Elevated phenotypic variance provides an insurance effect that increases the likelihood that some proportion of the population will be resistant to imposed selective agents and may thus enhance persistence of the biofilm. Accounting for evolutionary change in biofilms will improve our ability to understand and counter diseases that are caused by biofilm persistence.

Association mapping of local adaptation traits of Scots pine in a European wide population sample

Traits related to local adaptation by definition show high phenotypic differentiation. The underlying genetic patterns could be clines at individual loci or small effects and extensive linkage disequilibrium at the underlying loci. In any case, including many populations in an analysis provides more information, but may simultaneously induce problems due to genetic structure. Even if the neutral loci have little genetic structure, loci related to other clinally selected traits could show more structure. Here we have developed an approach to efficiently use the information along a latitudinal environmental gradient. Scots pine populations from central Europe to the species' northern range were sampled and patterns of phenotypic variation of both timing of budset and frost tolerance were measured in common garden experiments, (10 populations, a total of 270 halfsib families, 25 trees per family). By hierarchical modelling of the phenotype's clinal variation and accounting for varying allele frequencies across the 10 populations, the statistical approach simultaneously exploits the genetic variation between and within populations to detect association signals. We apply shrinkage-based Bayesian variable selection to detect genetic associations between timing of bud set and ~450 SNPs in Scots pine.

CONVERGENT EVOLUTION OF PHENOTYPIC INTEGRATION AND ITS ALIGNMENT WITH MORPHOLOGICAL DIVERSIFICATION IN CARIBBEAN ANOLIS ECOMORPHS

The adaptive landscape and the G-matrix are keys concepts for understanding how quantitative characters evolve during adaptive radiation. In particular, whether the adaptive landscape can drive convergence of phenotypic integration (i.e., the pattern of phenotypic variation and covariation summarized in the P-matrix) is not well studied. We estimated and compared P for 19 morphological traits in eight species of Caribbean Anolis lizards, finding that similarity in P among species was not correlated with phylogenetic distance. However, greater similarity in P among ecologically similar Anolis species (i.e., the trunk-ground ecomorph) suggests the role of convergent natural selection. Despite this convergence and relatively deep phylogenetic divergence, a large portion of eigenstructure of P is retained among our eight focal species. We also analyzed P as an approximation of G to test for correspondence with the pattern of phenotypic divergence in 21 Caribbean Anolis species. These patterns of covariation were coincident, suggesting that either genetic constraint has influenced the pattern of among-species divergence or, alternatively, that the adaptive landscape has influenced both G and the pattern of phenotypic divergence among species. We provide evidence for convergent evolution of phenotypic integration for one class of Anolis ecomorph, revealing yet another important dimension of evolutionary convergence in this group.

The sexual signals of the East-Mediterranean barn swallow: a different swallow tale

The differential functions of distinct morphological traits as sexual signals among closely related populations are associated with a potential role of sexual selection in population divergence and speciation. The cosmopolitan barn swallow Hirundo rustica complex consists of 6 subspecies, which differ substantially in tail streamer length and ventral coloration. Two of these subspecies—the European and North American subspecies—have been extensively studied. Though they are closely related, differentially exaggerated traits in these two subspecies appear to be the result of stronger sexual selection on tail length in Europe and ventral color in North America. The nonmigratory East-Mediterranean subspecies H. r. transitiva possesses both elongated long tail streamers and dark (brown-red) ventral coloration. We explored whether the expression of both traits is related to their potential role as sexual signals. In males, dark ventral coloration was the strongest predictor of breeding success, whereas tail streamer length was related to early breeding, and the likelihood of having multiple broods within a season. Older males, which typically have long streamers, were also less likely to have extrapair young in their nests. Tail streamer length and not ventral coloration predicted the breeding success of females. Considered in concert with earlier work on other populations, these findings show how patterns of phenotypic variation in the barn swallow species complex are underlain by differential sexual selection on tail length and ventral color, traits used variably among populations in mate choice and paternity decisions.

Geographic variation of floral traits in Nicotiana glauca: Relationships with biotic and abiotic factors

Geographic pattern of phenotypic variation can appear in a clinal or a mosaic fashion and can evidence adaptive or non-adaptive variation. To shed light on the mechanisms underlying this variation, we studied the relationships between geographic variation of floral traits and both biotic and abiotic factors of the hummingbird-pollinated plant, Nicotiana glauca, across its natural range. We obtained floral measures of 38 populations from an area about 1600 km long and 1050 km wide and an altitude range from 7 to over 3400 m. We used a MANOVA to detect between-population differentiations in flower traits and a DFA to determine the traits that best discriminate between populations. To test for associations between floral traits and climatic variables we used correlation analysis. We explored any possible distance-based pattern of variation (either geographic or altitudinal) in floral traits or bill length of pollinators using Mantel tests. Finally, we used a multiple regression to analyze simultaneously the effects and relative importance of abiotic predictor variables and bill length on corolla length. We found a high variation in flower traits among populations. Morphometric traits were the ones that best discriminated across populations. There was a clinal pattern of floral phenotypic variation explained by climatic factors. Differences in floral phenotypic distances were structured by altitudinal distances but not by geographic distances. Bill length of the hummingbird pollinators was structured both by altitudinal and geographic distances. Differences in bill length of hummingbird pollinators explained differences in corolla length across populations. Our findings support the assumption of flower evolution at a broad geographic scale. Floral traits seem to be structured not only by altitude but also by climatic factors.

Genetic and phenotypic variation in a colourful treefrog across five geographic barriers

Aim Understanding the patterns and processes underlying phenotype in a polytypic species provides key insights into microevolutionary mechanisms of diversification. The red-eyed treefrog, Agalychnis callidryas, exhibits strong regional differentiation in colour pattern, corresponding to five admixed mitochondrial DNA clades. We evaluated spatial diversity patterns across multiple, putative barriers to examine the fine-scale processes that mediate phenotypic divergence between some regions while maintaining homogeneity between others. Location We examined patterns of phenotypic diversification among 17 sites that span five putative biogeographic barriers in lower Central America (Costa Rica and Panama). Methods We tested the extent to which genetic distance (FST) derived from six multilocus nuclear genotypes covaried with measures of phenotypic distance (leg coloration) within and between biogeographic regions. We used linear regression analyses to determine the role of geographic and genetic factors in structuring spatial patterns of phenotypic diversity. Results The factors that best explained patterns of phenotypic diversity varied among biogeographic regions. We identified one geographic barrier that impeded gene exchange and resulted in concordant phenotypic divergence across the Continental Divide, isolating Caribbean and Pacific populations. Across Caribbean Costa Rican populations, one barrier structured phenotypic but not genetic diversity patterns, indicating a role for selection. In other regions, the putative barriers had no determining effect on either genetic or leg colour structure. Main conclusions The processes mediating the distribution and diversification of colour pattern in this polytypic, wide-ranging treefrog varied among biogeographic regions. Spatially varying selection combined with the isolating effects of geographic factors probably resulted in the patchy distribution of colour diversity across Costa Rican and Panamanian populations.