Patrice David

Mapping phenotypes: canalization, plasticity and developmental stability

The relationship between genotype and phenotype is not one to one. This statement is central to our understanding of how natural selection shapes phenotypic evolution. Here, we clarify the links between canalization, plasticity and developmental stability, the three major processes involved in the control of phenotypic variability. We present a short historical review, including the original definitions of these concepts, and then summarize their current meaning and use, highlighting possible sources of confusion. Some of the perspectives allowed by a more synthetic conceptual framework are presented, in the light of the recent advances in molecular and developmental genetics.

The coupling hypothesis: why genome scans may fail to map local adaptation genes

Genomic scans of multiple populations often reveal marker loci with greatly increased differentiation between populations. Often this differentiation coincides in space with contrasts in ecological factors, forming a genetic–environment association (GEA). GEAs imply a role for local adaptation, and so it is tempting to conclude that the strongly differentiated markers are themselves under ecologically based divergent selection, or are closely linked to loci under such selection. Here, we highlight an alternative and neglected explanation: intrinsic (i.e. environment‐independent) pre‐ or post‐zygotic genetic incompatibilities rather than local adaptation can be responsible for increased differentiation. Intrinsic genetic incompatibilities create endogenous barriers to gene flow, also known as tension zones, whose location can shift over time. However, tension zones have a tendency to become trapped by, and therefore to coincide with, exogenous barriers due to ecological selection. This coupling of endogenous and exogenous barriers can occur easily in spatially subdivided populations, even if the loci involved are unlinked. The result is that local adaptation explains where genetic breaks are positioned, but not necessarily their existence, which can be best explained by endogenous incompatibilities. More precisely, we show that (i) the coupling of endogenous and exogenous barriers can easily occur even when ecological selection is weak; (ii) when environmental heterogeneity is fine‐grained, GEAs can emerge at incompatibility loci, but only locally, in places where habitats and gene pools are sufficiently intermingled to maintain linkage disequilibria between genetic incompatibilities, local‐adaptation genes and neutral loci. Furthermore, the association between the locally adapted and intrinsically incompatible alleles (i.e. the sign of linkage disequilibrium between endogenous and exogenous loci) is arbitrary and can form in either direction. Reviewing results from the literature, we find that many predictions of our model are supported, including endogenous genetic barriers that coincide with environmental boundaries, local GEA in mosaic hybrid zones, and inverted or modified GEAs at distant locations. We argue that endogenous genetic barriers are often more likely than local adaptation to explain the majority of Fst‐outlying loci observed in genome scan approaches – even when these are correlated to environmental variables.

HETEROZYGOSITY-FITNESS CORRELATIONS : NEW PERSPECTIVES ON OLD PROBLEMS

Heterozygosity–fitness correlations (HFC) have been studied in various organisms for more than two decades, but they are not universal. Although their detectability is limited by several factors (null alleles, inaccuracy of the phenotypic description of fitness, small sample sizes) the correlations appear intrinsically weak and often inconsistent across samples. Determining the origins of HFC is therefore a complex task. However, this issue might soon be resolved provided clear hypotheses and definitions are used (especially, if the problem of the neutrality of allozyme variation is not identified with the related issue of HFC), as well as new empirical (molecular markers) & theoretical (statistical models) tools.

Reliable selfing rate estimates from imperfect population genetic data

Genotypic frequencies at codominant marker loci in population samples convey information on mating systems. A classical way to extract this information is to measure heterozygote deficiencies (FIS) and obtain the selfing rate s from FIS = s/(2 − s), assuming inbreeding equilibrium. A major drawback is that heterozygote deficiencies are often present without selfing, owing largely to technical artefacts such as null alleles or partial dominance. We show here that, in the absence of gametic disequilibrium, the multilocus structure can be used to derive estimates of s independent of FIS and free of technical biases. Their statistical power and precision are comparable to those of FIS, although they are sensitive to certain types of gametic disequilibria, a bias shared with progeny‐array methods but not FIS. We analyse four real data sets spanning a range of mating systems. In two examples, we obtain s = 0 despite positive FIS, strongly suggesting that the latter are artefactual. In the remaining examples, all estimates are consistent. All the computations have been implemented in a open‐access and user‐friendly software called rmes (robust multilocus estimate of selfing) available at http://ftp.cefe.cnrs.fr, and can be used on any multilocus data. Being able to extract the reliable information from imperfect data, our method opens the way to make use of the ever‐growing number of published population genetic studies, in addition to the more demanding progeny‐array approaches, to investigate selfing rates.

HETEROZYGOSITY-FITNESS CORRELATIONS: A TIME FOR REAPPRAISAL

Owing to the remarkable progress of molecular techniques, heterozygosity‐fitness correlations (HFCs) have become a popular tool to study the impact of inbreeding in natural populations. However, their underlying mechanisms are often hotly debated. Here we argue that these “debates” rely on verbal arguments with no basis in existing theory and inappropriate statistical testing, and that it is time to reconcile HFC with its historical and theoretical fundaments. We show that available data are quantitatively and qualitatively consistent with inbreeding‐based theory. HFC can be used to estimate the impact of inbreeding in populations, although such estimates are bound to be imprecise, especially when inbreeding is weak. Contrary to common belief, linkage disequilibrium is not an alternative to inbreeding, but rather comes with some forms of inbreeding, and is not restricted to closely linked loci. Finally, the contribution of local chromosomal effects to HFC, while predicted by inbreeding theory, is expected to be small, and has rarely if ever proven statistically significant using adequate tests. We provide guidelines to safely interpret and quantify HFCs, and present how HFCs can be used to quantify inbreeding load and unravel the structure of natural populations.

High Genetic Variance in Life-History Strategies within Invasive Populations by Way of Multiple Introductions

Biological invasions represent major threats to biodiversity as well as large-scale evolutionary experiments. Invasive populations have provided some of the best known examples of contemporary evolution [3-6], challenging the classical view that invasive species are genetically depauperate because of founder effects. Yet the origin of trait genetic variance in invasive populations largely remains a mystery, precluding a clear understanding of how evolution proceeds. In particular, despite the emerging molecular evidence that multiple introductions commonly occur in the same place, their contribution to the evolutionary potential of invasives remains unclear. Here, by using a long-term field survey, mtDNA sequences, and a large-scale quantitative genetic experiment on freshwater snails, we document how a spectacular adaptive potential for key ecological traits can be accumulated in invasive populations. We provide the first direct evidence that multiple introductions are primarily responsible for such an accumulation and that sexual reproduction amplifies this effect by generating novel trait combinations. Thus bioinvasions, destructive as they may be, are not synonyms of genetic uniformity and can be hotspots of evolutionary novelty.

Introgression patterns in the mosaic hybrid zone between Mytilus edulis and M. galloprovincialis

Hybrid zones are fascinating systems to investigate the structure of genetic barriers. Marine hybrid zones deserve more investigation because of the generally high dispersion potential of planktonic larvae which allows migration on scales unrivalled by terrestrial species. Here we analyse the genetic structure of the mosaic hybrid zone between the marine mussels Mytilus edulis and M. galloprovincialis, using three length‐polymorphic PCR loci as neutral and diagnostic markers on 32 samples along the Atlantic coast of Europe. Instead of a single genetic gradient from M. galloprovincialis on the Iberian Peninsula to M. edulis populations in the North Sea, three successive transitions were observed in France. From South to North, the frequency of alleles typical of M. galloprovincialis first decreases in the southern Bay of Biscay, remains low in Charente, then increases in South Brittany, remains high in most of Brittany, and finally decreases again in South Normandy. The two enclosed patches observed in the midst of the mosaic hybrid zone in Charente and Brittany, although predominantly M. edulis‐like and M. galloprovincialis‐like, respectively, are genetically original in two respects. First, considering only the various alleles typical of one species, the patches show differentiated frequencies compared to the reference external populations. Second, each patch is partly introgressed by alleles of the other species. When introgression is taken into account, linkage disequilibria appear close to their maximum possible values, indicating a strong genetic barrier within all transition zones. Some pre‐ or postzygotic isolation mechanisms (habitat specialization, spawning asynchrony, assortative fertilization and hybrid depression) have been documented in previous studies, although their relative importance remains to be evaluated. We also provided evidence for a recent migratory ‘short‐cut’ connecting M. edulis‐like populations of the Charente patch to an external M. edulis population in Normandy and thought to reflect artificial transfer of spat for aquaculture.

A review of relationships between interspecific competition and invasions in fruit flies (Diptera : Tephritidae)

Abstract.  1. A number of invasions in the family Tephritidae (fruit flies) have been observed worldwide despite quarantine procedures. In this review, the potential importance of interspecific competition and competitive displacement among different tephritid species is evaluated in the context of recent invasions.

Independence between developmental stability and canalization in the skull of the house mouse

The relationship between the two components of developmental homeostasis, that is canalization and developmental stability (DS), is currently debated. To appraise this relationship, the levels and morphological patterns of interindividual variation and fluctuating asymmetry were assessed using a geometric morphometric approach applied to the skulls of laboratory samples of the house mouse. These three samples correspond to two random–bred strains of the two European subspecies of the house mouse and their F1 hybrids. The inter– and intraindividual variation levels were found to be smaller in the hybrid group compared to the parental ones, suggesting a common heterotic effect on skull canalization and DS. Both buffering mechanisms might then depend on the same genetic condition, i.e. the level of heterozygosity. However, related morphological patterns did not exhibit any congruence. In contradiction with previous studies on insect wing traits, we therefore suggest that canalization and DS may not act on the same morphological characters. The fact that this discrepancy could be related to the functional importance of the symmetry of the characters under consideration is discussed in the light of our knowledge of the genetic bases of both components of developmental homeostasis.

Hybridization and invasiveness in the freshwater snail Melanoides tuberculata: hybrid vigour is more important than increase in genetic variance.

Many invasive taxa are hybrids, but how hybridization boosts the invasive process remains poorly known. We address this question in the clonal freshwater snail Melanoides tuberculata from Martinique, using three parental and two hybrid lines. We combine an extensive field survey (1990–2003) and a quantitative genetic experiment to show that hybrid lines have outcompeted their parents in natural habitats, and that this increased invasiveness co‐occurred with pronounced shifts in life‐history traits, such as growth, fecundity and juvenile size. Given the little time between hybrid creation and sampling, and the moderate standing genetic variance for life‐history traits in hybrids, we show that some of the observed trait changes between parents and hybrids were unlikely to arise only by continuous selection. We therefore suggest that a large part of hybrid advantage stems from immediate heterosis upon hybridization.