Testing the molecular and evolutionary causes of a 'leapfrog' pattern of geographical variation in coloration

Understanding the mechanisms accounting for the evolution of phenotypic diversity is central to evolutionary biology. We use molecular and phenotypic data to test hypotheses for 'leapfrog' patterns of geographical variation, in which phenotypically similar, disjunct populations are separated by distinct populations of the same species. Phylogenetic reconstructions revealed independent evolution of melanic plumage characters in different populations in the Neotropical avian genus Arremon. Thus, phenotypic similarities between distant populations cannot be explained by close phylogenetic affinity. Nor can they be attributed to recurring mutations in the MC1R gene, a locus involved in melanic pigmentation. A coalescent analysis indicates that plumage traits have become fixed at a faster rate than expected under genetic drift, suggesting that selection underlies their repeated evolution. In contrast to views that genetic drift drives phenotypic differentiation in Neotropical montane birds, our results imply that geographical variation preceding speciation may reflect the action of deterministic selective processes.     

Sexual size dimorphism and sexual selection in primates

1. In most animals, females are larger than males. Paradoxically, sexual size dimorphism is biased towards males in most mammalian species. An accepted explanation is that sexual dimorphism in mammals evolved by intramale sexual selection. I tested this hypothesis in primates, by relating sexual size dimorphism to seven proxies of sexual selection intensity: operational sex ratio, mating system, intermale competition, group sex ratio, group size, maximum mating percentage (percentage of observed copulations involving the most successful male), and total paternity (a genetic estimate of the percentage of young sired by the most successful male).
2. I fitted phylogenetic generalised least squares models using sexual size dimorphism as the dependent variable and each of the seven measures of intensity of sexual selection as independent variables. I conducted this comparative analysis with data from 50 extant species of primates, including Homo sapiens, Pan troglodytes, and Gorilla spp.
3. Sexual dimorphism was positively related to the four measures of female monopolisation (operational sex ratio, mating system, intermale competition, and group sex ratio) and in some cases to group size, but was not associated with maximum mating percentage or total paternity. Additional regression analyses indicated that maximum mating percentage and total paternity were negatively associated with group size.
4. These results are predicted by reproductive skew theory: in large groups, males can lose control of the sexual behaviour of the other members of the group or can concede reproductive opportunities to others. The results are also consistent with the evolution of sexual size dimorphism before polygyny, due to the effects of natural, rather than sexual, selection. In birds, the study of molecular paternity showed that variance in male reproductive success is much higher than expected by behaviour. In mammals, recent studies have begun to show the opposite trend, i.e. that intensity of sexual selection is lower than expected by polygyny.
5. Results of this comparative analysis of sexual size dimorphism and sexual selection intensity in primates suggest that the use of intramale sexual selection theory to explain the evolution of polygyny and sexual dimorphism in mammals should be reviewed, and that natural selection should be considered alongside sexual selection as an evolutionary driver of sexual size dimorphism and polygyny in mammals.

     

Sexual selection and the evolutionary dynamics of the major histocompatibility complex

The genes of the major histocompatibility complex (MHC) are a key component of the adaptive immune system and among the most variable loci in the vertebrate genome. Pathogen-mediated natural selection and MHC-based disassortative mating are both thought to structure MHC polymorphism, but their effects have proven difficult to discriminate in natural systems. Using the first model of MHC dynamics incorporating both survival and reproduction, we demonstrate that natural and sexual selection produce distinctive signatures of MHC allelic diversity with critical implications for understanding host–pathogen dynamics. While natural selection produces the Red Queen dynamics characteristic of host–parasite interactions, disassortative mating stabilizes allele frequencies, damping major fluctuations in dominant alleles and protecting functional variants against drift. This subtle difference generates a complex interaction between MHC allelic diversity and population size. In small populations, the stabilizing effects of sexual selection moderate the effects of drift, whereas pathogen-mediated selection accelerates the loss of functionally important genetic diversity. Natural selection enhances MHC allelic variation in larger populations, with the highest levels of diversity generated by the combined action of pathogen-mediated selection and disassortative mating. MHC-based sexual selection may help to explain how functionally important genetic variation can be maintained in populations of conservation concern.     

Points of view: Cannibalism and OSR -- a response to Kvarnemo

Reviews in Fish Biology and Fisheries -     

Points of view: Why male cannibalism won't cause a female-biased OSR -- a comment on Smith and Wootton's paper

Reviews in Fish Biology and Fisheries -     

Migration and the evolution of sexual dichromatism: evolutionary loss of female coloration with migration among wood-warblers

The mechanisms underlying evolutionary changes in sexual dimorphism have long been of interest to biologists. A striking gradient in sexual dichromatism exists among songbirds in North America, including the wood-warblers (Parulidae): males are generally more colourful than females at northern latitudes, while the sexes are similarly ornamented at lower latitudes. We use phylogenetically controlled comparative analysis to test three non-mutually exclusive hypotheses for the evolution of sexual dichromatism among wood-warblers. The first two hypotheses focus on the loss of female coloration with the evolution of migration, either owing to the costs imposed by visual predators during migration, or owing to the relaxation of selection for female social signalling at higher latitudes. The third hypothesis focuses on whether sexual dichromatism evolved owing to changes in male ornamentation as the strength of sexual selection increases with breeding latitude. To test these hypotheses, we compared sexual dichromatism to three variables: the presence of migration, migration distance, and breeding latitude. We found that the presence of migration and migration distance were both positively correlated with sexual dichromatism, but models including breeding latitude alone were not strongly supported. Ancestral state reconstruction supports the hypothesis that the ancestral wood-warblers were monochromatic, with both colourful males and females. Combined, these results are consistent with the hypotheses that the evolution of migration is associated with the relaxation of selection for social signalling among females and that there are increased predatory costs along longer migratory routes for colourful females. These results suggest that loss of female ornamentation can be a driver of sexual dichromatism and that social or natural selection may be a stronger contributor to variation in dichromatism than sexual selection.     

The effect of habitat fragmentation on the genetic structure of a top predator: loss of diversity and high differentiation among remnant populations of Atlantic Forest jaguars (Panthera onca)

Habitat fragmentation may disrupt original patterns of gene flow and lead to drift-induced differentiation among local population units. Top predators such as the jaguar may be particularly susceptible to this effect, given their low population densities, leading to small effective sizes in local fragments. On the other hand, the jaguar's high dispersal capabilities and relatively long generation time might counteract this process, slowing the effect of drift on local populations over the time frame of decades or centuries. In this study, we have addressed this issue by investigating the genetic structure of jaguars in a recently fragmented Atlantic Forest region, aiming to test whether loss of diversity and differentiation among local populations are detectable, and whether they can be attributed to the recent effect of drift. We used 13 microsatellite loci to characterize the genetic diversity present in four remnant populations, and observed marked differentiation among them, with evidence of recent allelic loss in local areas. Although some migrant and admixed individuals were identified, our results indicate that recent large-scale habitat removal and fragmentation among these areas has been sufficiently strong to promote differentiation induced by drift and loss of alleles at each site. Low estimated effective sizes supported the inference that genetic drift could have caused this effect within a short time frame. These results indicate that jaguars' ability to effectively disperse across the human-dominated landscapes that separate the fragments is currently very limited, and that each fragment contains a small, isolated population that is already suffering from the effects of genetic drift.     

Beyond sex,gender, and other dilemmas: Human pelvic morphology from an integrative context

Recent research on the pelvis has clarified the flexibility of pelvic bones to manage nearly infinite possibilities in terms of selection and drift, while still maintaining excellent bipedalism. Despite this work, and the studies outlining the diversity of pelvic morphology across the hominin lineage, conversations continue to be stymied by distractions related to purported trade-offs that the different functions the pelvis must either allow for (e.g., parturition) or directly perform (e.g., attachment sites of muscles). Here we show that tight constraints on morphology are not evident in the pelvic variation of multiple human populations. We thus provide further evidence that human pelves are not geometrically similar and that pelvic morphology successfully balances the intersection of population history, active selective, and drift.     

Redundancy analysis,genome-wide association studies and the pigmentation of brown trout (Salmo trutta L.)

The association of molecular variants with phenotypic variation is a main issue in biology, often tackled with genome-wide association studies (GWAS). GWAS are challenging, with increasing, but still limited, use in evolutionary biology. We used redundancy analysis (RDA) as a complimentary ordination approach to single- and multitrait GWAS to explore the molecular basis of pigmentation variation in brown trout (Salmo trutta) belonging to wild populations impacted by hatchery fish. Based on 75,684 single nucleotide polymorphic (SNP) markers, RDA, single- and multitrait GWAS allowed the extraction of 337 independent colour patterning loci (CPLs) associated with trout pigmentation traits, such as the number of red and black spots on flanks. Collectively, these CPLs (i) mapped onto 35 out of 40 brown trout linkage groups indicating a polygenic genomic architecture of pigmentation, (ii) were found to be associated with 218 candidate genes, including 197 genes formerly mentioned in the literature associated to skin pigmentation, skin patterning, differentiation or structure notably in a close relative, the rainbow trout (Onchorhynchus mykiss), and (iii) related to functions relevant to pigmentation variation (e.g., calcium- and ion-binding, cell adhesion). Annotated CPLs include genes with well-known pigmentation effects (e.g., PMEL, SLC45A2, SOX10), but also markers associated with genes formerly found expressed in rainbow or brown trout skins. RDA was also shown to be useful to investigate management issues, especially the dynamics of trout pigmentation submitted to several generations of hatchery introgression.     

Local adaptation and matching habitat choice in female barn owls with respect to melanic coloration

Local adaptation is a major mechanism underlying the maintenance of phenotypic variation in spatially heterogeneous environments. In the barn owl (Tyto alba), dark and pale reddish-pheomelanic individuals are adapted to conditions prevailing in northern and southern Europe, respectively. Using a long-term dataset from Central Europe, we report results consistent with the hypothesis that the different pheomelanic phenotypes are adapted to specific local conditions in females, but not in males. Compared to whitish females, reddish females bred in sites surrounded by more arable fields and less forests. Colour-dependent habitat choice was apparently beneficial. First, whitish females produced more fledglings when breeding in wooded areas, whereas reddish females when breeding in sites with more arable fields. Second, cross-fostering experiments showed that female nestlings grew wings more rapidly when both their foster and biological mothers were of similar colour. The latter result suggests that mothers should particularly produce daughters in environments that best match their own coloration. Accordingly, whiter females produced fewer daughters in territories with more arable fields. In conclusion, females displaying alternative melanic phenotypes bred in habitats providing them with the highest fitness benefits. Although small in magnitude, matching habitat selection and local adaptation may help maintain variation in pheomelanin coloration in the barn owl.     

The mismeasurement of sexual selection

Sexual selection can explain major micro‐ and macro‐evolutionary patterns. Much of current theory predicts that the strength of sexual selection (i) is driven by the relative abundance of males and females prepared to mate (i.e. the operational sex ratio, OSR) and (ii) can be generally estimated by calculating intra‐sexual variation in mating success (e.g. the opportunity for sexual selection, I_s). Here, we demonstrate the problematic nature of these predictions. The OSR and I_s only accurately predict sexual selection under a limited set of circumstances, and more specifically, only when mate monopolization is extremely strong. If mate monopolization is not strong, using OSR or I_s as proxies or measures of sexual selection is expected to produce spurious results that lead to the false conclusion that sexual selection is strong when it is actually weak. These findings call into question the validity of empirical conclusions based on these measures of sexual selection.     

Drift happens: Molecular genetic diversity and differentiation among populations of jewelweed (Impatiens capensis Meerb.) reflect fragmentation of floodplain forests

Landscape features often shape patterns of gene flow and genetic differentiation in plant species. Populations that are small and isolated enough also become subject to genetic drift. We examined patterns of gene flow and differentiation among 12 floodplain populations of the selfing annual jewelweed (Impatiens capensis Meerb.) nested within four river systems and two major watersheds in Wisconsin, USA. Floodplain forests and marshes provide a model system for assessing the effects of habitat fragmentation within agricultural/urban landscapes and for testing whether rivers act to genetically connect dispersed populations. We generated a panel of 12,856 single nucleotide polymorphisms and assessed genetic diversity, differentiation, gene flow, and drift. Clustering methods revealed strong population genetic structure with limited admixture and highly differentiated populations (mean multilocus F_ST = 0.32, F_ST’ = 0.33). No signals of isolation by geographic distance or environment emerged, but alleles may flow along rivers given that genetic differentiation increased with river distance. Differentiation also increased in populations with fewer private alleles (R² = 0.51) and higher local inbreeding (R² = 0.22). Populations varied greatly in levels of local inbreeding (F_IS = 0.2–0.9) and F_IS increased in more isolated populations. These results suggest that genetic drift dominates other forces in structuring these Impatiens populations. In rapidly changing environments, species must migrate or genetically adapt. Habitat fragmentation limits both processes, potentially compromising the ability of species to persist in fragmented landscapes.     

Book review of evolutionary genetics: Concepts,analysis, and practice

Recent technological advances have expanded and increased the resolution of studies in evolutionary biology, creating a need for a modern textbook that highlights the latest developments in the field. Evolutionary Genetics: Concepts, Analysis, and Practice, by Glenn‐Peter Sætre and Mark Ravinet (2019), as well as the book's accompanying online tutorials, provide a clear, up‐to‐date, and enjoyable introduction to evolutionary biology and genetics that explains fundamental evolutionary concepts, illustrates recent exciting findings, and offers hands‐on experience in analysing and interpreting genomic data. The book's accessible nature and emphasis on developing practical skills make it a valuable resource for undergraduate courses on evolutionary biology.     

Variation in sexual reproduction in orchids and its evolutionary consequences: a spasmodic journey to diversification

The great taxonomic diversity of the Orchidaceae is often attributed to adaptive radiation for specific pollinators driven by selection for outcrossing. However, when one looks beyond the product to the process, the evidence for selection is less than overwhelming. We explore this problem by discussing relevant aspects of orchid biology and asking which aspects of reproduction explain the intricate pollination mechanisms and diversification of this family. We reaffirm that orchids are primarily pollination limited, the severity of which is affected by resource constraints. Fruit set is higher in temperate than in tropical species, and in species which offer pollinator rewards than those that do not. Reproductive success is skewed towards few individuals in a population and effective population sizes are often small. Population structure, reproductive success and gene flow among populations suggest that in many situations genetic drift may be as important as selection in fostering genetic and morphological variation in this family. Although there is some evidence for a gradualist model of evolutionary change, we believe that the great diversity in this family is largely a consequence of sequential and rapid interplay between drift and natural selection.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 84 , 1–54.     

The consequences of sexual selection in well‐adapted and maladapted populations of bean beetles†

Whether sexual selection generally promotes or impedes population persistence remains an open question. Intralocus sexual conflict (IaSC) can render sexual selection in males detrimental to the population by increasing the frequency of alleles with positive effects on male reproductive success but negative effects on female fecundity. Recent modeling based on fitness landscape theory, however, indicates that the relative impact of IaSC may be reduced in maladapted populations and that sexual selection therefore might promote adaptation when it is most needed. Here, we test this prediction using bean beetles that had undergone 80 generations of experimental evolution on two alternative host plants. We isolated and assessed the effect of maladaptation on sex‐specific strengths of selection and IaSC by cross‐rearing the two experimental evolution regimes on the alternative hosts and estimating within‐population genetic (co)variance for fitness in males and females. Two key predictions were upheld: males generally experienced stronger selection compared to females and maladaptation increased selection in females. However, maladaptation consistently decreased male‐bias in the strength of selection and IaSC was not reduced in maladapted populations. These findings imply that sexual selection can be disrupted in stressful environmental conditions, thus reducing one of the potential benefits of sexual reproduction in maladapted populations.     

栖息地片断化对动物种群间基因流的影响及其测定方法

栖息地片断化指在人为活动和自然干扰下,大面积连续分布的自然栖息地被其它非适宜栖息地分隔成许多面积较小的斑块(岛屿)的过程。栖息地片断化是导致生物多样性丧失和物种绝灭的主要因素,也是威胁自然界生物生存的重要因素之一。栖息地片断化将影响基因在种群间和种群内的运动(基因流),开展栖息地片断化研究对保持物种间遗传多样性具有重要意义。本文介绍了片断化程度和基因流的测定方法。回顾了国内外的研究现状,并探讨了片断化对种群间基因流的影响和对濒危物种保护的意义。     

Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches

Conservation of genetic diversity, one of the three main forms of biodiversity, is a fundamental concern in conservation biology as it provides the raw material for evolutionary change and thus the potential to adapt to changing environments. By means of meta‐analyses, we tested the generality of the hypotheses that habitat fragmentation affects genetic diversity of plant populations and that certain life history and ecological traits of plants can determine differential susceptibility to genetic erosion in fragmented habitats. Additionally, we assessed whether certain methodological approaches used by authors influence the ability to detect fragmentation effects on plant genetic diversity. We found overall large and negative effects of fragmentation on genetic diversity and outcrossing rates but no effects on inbreeding coefficients. Significant increases in inbreeding coefficient in fragmented habitats were only observed in studies analyzing progenies. The mating system and the rarity status of plants explained the highest proportion of variation in the effect sizes among species. The age of the fragment was also decisive in explaining variability among effect sizes: the larger the number of generations elapsed in fragmentation conditions, the larger the negative magnitude of effect sizes on heterozygosity. Our results also suggest that fragmentation is shifting mating patterns towards increased selfing. We conclude that current conservation efforts in fragmented habitats should be focused on common or recently rare species and mainly outcrossing species and outline important issues that need to be addressed in future research on this area.     

Operational sex ratio, sexual conflict and the intensity of sexual selection

Modern sexual selection theory indicates that reproductive costs rather than the operational sex ratio predict the intensity of sexual selection. We investigated sexual selection in the polygynandrous common lizard Lacerta vivipara . This species shows male aggression, causing high mating costs for females when adult sex ratios (ASR) are male-biased. We manipulated ASR in 12 experimental populations and quantified the intensity of sexual selection based on the relationship between reproductive success and body size. In sharp contrast to classical sexual selection theory predictions, positive directional sexual selection on male size was stronger and positive directional selection on female size weaker in female-biased populations than in male-biased populations. Thus, consistent with modern theory, directional sexual selection on male size was weaker in populations with higher female mating costs. This suggests that the costs of breeding, but not the operational sex ratio, correctly predicted the strength of sexual selection.     

Limits to sexual size dimorphism in red‐winged blackbirds: the cost of getting big?

A fundamental assumption of sexual selection theory is that the reproductive advantage of large size is balanced by a survival disadvantage. Previous studies of the sexually size-dimorphic red-winged blackbird ( Agelaius phoeniceus ) have indicated that the largest adult males have a survival advantage, suggesting that the limit to male size may be the cost of getting big rather than the cost of being big. If the cost of getting big limits male size, then starvation rates for male nestlings should exceed those of female nestlings. In addition, given high heritability of body size, larger parents should lose more nestlings, particularly males, to starvation. We tested these predictions for red-winged blackbirds using data on the sex of 1356 fledglings from 465 nests collected over 10 years. We found no disadvantage for male nestlings relative to females – 49% of fledglings were male and previous research had shown that 48% of hatchlings are male. We also found no disadvantage for male nestlings that would become large adults (i.e. those with larger parents) – partial brood loss and fledging sex ratios did not vary with mid-parent size. Given no apparent disadvantage to large size for males either as adults or as nestlings, this leaves only the period between fledging and adulthood during which natural selection might limit sexual size dimorphism, although other mechanisms might explain the failure to find a limit to male size.  © 2005 The Linnean Society of London, Biological Journal of the Linnean Society , 2005, 85 , 353–361.     

Population differences in the roles of size and coloration in intra-and intersexual selection in the collared lizard, Crotaphytus collaris: influence of habitat and social organization

Previous studies have shown that in three Oklahoma populationsof collared lizards, Wichita Mountains (WM), Glass Mountains(GM), and Arcadia Lake (AL), sexual dimorphism in body sizevaries as WM>AL>GM, whereas dorsal color dimorphism variesas GM>WM>AL. Social organization at these sites also differssuch that the environmental potential for sexual selection variesas AL>WM>GM. We conducted female choice and male competitionlaboratory trials to assess whether advantages to large or brightmales correlate best with the interpopulation pattern of sexualdimorphism or with that of the environmental potential for sexualselection. Between-population trials involved bright-coloredWM males and dull-colored AL males that were matched for size.AL females preferred bright WM males, but WM females did not.WM males had higher agonistic scores in intrasexual contestswhen aggression was low, but AL males consistently had higherscores when aggression escalated. Within-population trials involvedmales that were disparate in color but size matched and disparatein size but color matched. Size was important in male contestsin all populations. Color brightness was a factor in male trialsonly at AL. Also, only AL females preferred brighter males,and larger males were not preferred in any population. The importanceof intra and intersexual selection in these populations cannotbe inferred from the observed pattern of size and color dimorphism.Rather, interpopulation differences in the environmental potentialfor females to assess and choose from among multiple males,and for males to interact, are most consistent with the observedoutcomes.