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Self-fertilization is expected to reduce genetic diversity within populations and consequently to limit adaptability to changing environments. Little is known, however, about the way the evolution of self-fertilization changes the amount or pattern of the components of genetic variation in natural populations. In this study, a reciprocal North Carolina II design and maximum-likelihood methods were implemented to investigate the genetic basis of variation for 15 floral and vegetative traits in four populations of the annual plant Amsinckia spectabilis (Boraginaceae) differing in mating system. Six variance components were estimated according to Cockerham and Weir's “bio” model c. Compared to the three partially selfing populations, we found significantly lower levels of nuclear variance for several traits in the nearly completely self-fertilizing population. Furthermore, for 11 of 15 traits we did not detect nuclear variation to be significantly greater than zero. We also found high maternal variance in one of the partially selfing populations for several traits, and little dominance variance in any population. These results are in agreement with the evolutionary dead-end hypothesis for highly self-fertilizing taxa.
Epigenetic effects attributed to genomic imprinting are increasingly recognized as an important source of variation in quantitative traits. However, little is known about their relative contribution to phenotypic variation compared to those of additive and dominance effects, and almost nothing about their role in phenotypic evolution. Here we address these questions by investigating the relative contribution of additive, dominance, and imprinting effects of quantitative trait loci (QTL) to variation in “early” and “late” body weight in an intercross of mice selected for divergent adult body weight. We identified 18 loci on 13 chromosomes; additive effects accounted for most of the phenotypic variation throughout development, and imprinting effects were always small. Genetic effects on early weight showed more dominance, less additive, and, surprisingly, less imprinting variation than that of late weight. The predominance of additivity of QTL effects on body weight follows the expectation that additive effects account for the evolutionary divergence between selection lines. We hypothesize that the appearance of more imprinting effects on late body weight may be a consequence of divergent selection on adult body weight, which may have indirectly selected for alleles showing partial imprinting effects due to their associated additive effects, highlighting a potential role of genomic imprinting in the response to selection.
In mosses, separate and combined sexes are evolutionarily labile, yet factors selecting for this variation are unknown. In this study, we investigate phylogenetic correlations between sexual system and five life-history traits (asexual reproduction, chromosome number, gametophore length, spore size, and seta length). We assigned states to species on a large-scale phytogeny of mosses and used maximum likelihood analyses to test for the correlations and investigate the sequence of trait acquisition. Mosses in lineages with separate sexes were significantly more likely to be large, whereas those in lineages with combined sexes had higher chromosome numbers. Moreover, evolutionary transitions to separate sexes were more likely to occur in lineages with small spores. There was no support for a correlation between asexual reproduction and separate sexes. These results suggest that sexual system evolution is influenced by traits affecting mate availability and the dispersal of gametes and spores, and provides evidence for the existence of syndromes of life-history traits in mosses.
Many evolutionary studies require an understanding of phenotypic change. However, while analyses of phenotypic variation across pairs of evolutionary levels (populations or time steps) are well established, methods for testing hypotheses that compare evolutionary sequences across multiple levels are less developed. Here we describe a general analytical procedure for quantifying and comparing patterns of phenotypic evolution. The phenotypic evolution of a lineage is defined as a trajectory across a set of evolutionary levels in a multivariate phenotype space. Attributes of these trajectories (their size, direction, and shape), are quantified, and statistically compared across pairs of taxa, and a summary statistic is used to determine the extent to which patterns of phenotypic evolution are concordant across multiple taxa. This approach provides a direct quantitative description of how patterns of phenotypic evolution differ, as well as a statistical assessment of the degree of repeatability in the evolutionary responses to selection among taxa. We describe how this approach can quantify phenotypic trajectories from many ecological and evolutionary processes, whose data encode multivariate characterizations of the phenotype, including: phenotypic plasticity, ecological selection, ontogeny and growth, local adaptation, and biomechanics. We illustrate the approach by examining the phenotypic evolution of several fossil lineages of Globorotalia.
Theoretical models suggest that geographic overlap with different heterospecific assemblages can promote divergence of mate recognition systems among conspecific populations. Divergence occurs when different traits undergo reproductive character displacement across populations within a contact zone. Here, I tested this hypothesis by assessing patterns of acoustic signal divergence in two- and three-species assemblages of chorus frogs (Pseudacris), focusing in particular on P. feriarum and P. nigrita. In addition, I tested one criterion for reinforcement, by examining the evolution of female P. feriarum preferences in the contact zone. Patterns of signal evolution indicated that in each of the four sympatric populations studied, only the rarer species displaced substantially (P. feriarum in three cases and P. nigrita in one instance). Moreover, the three displaced P. feriarum populations diverged in different signal traits across the contact zone, evolving in directions that increased the energetic cost of calling relative to the allopatric call, and in ways that maximized differences from the particular heterospecific assemblage present. Consistent with reinforcement, divergence of female preferences in sympatry was estimated to reduce their propensity to hybridize by 60%. Together, signal and preference data suggest that interactions between species can promote diversification within species, potentially contributing to reproductive isolation among conspecific populations.
Felsenstein distinguished two ways by which selection can directly strengthen isolation. First, a modifier that strengthens prezygotic isolation can be favored everywhere. This fits with the traditional view of reinforcement as an adaptation to reduce deleterious hybridization by strengthening assortative mating. Second, selection can favor association between different incompatibilities, despite recombination. We generalize this “two allele” model to follow associations among any number of incompatibilities, which may include both assortment and hybrid inviability. Our key argument is that this process, of coupling between incompatibilities, may be quite different from the usual view of reinforcement: strong isolation can evolve through the coupling of any kind of incompatibility, whether prezygotic or postzygotic. Single locus incompatibilities become coupled because associations between them increase the variance in compatibility, which in turn increases mean fitness if there is positive epistasis. Multiple incompatibilities, each maintained by epistasis, can become coupled in the same way. In contrast, a single-locus incompatibility can become coupled with loci that reduce the viability of haploid hybrids because this reduces harmful recombination. We obtain simple approximations for the limits of tight linkage, and strong assortment, and show how assortment alleles can invade through associations with other components of reproductive isolation.
Hybridization between divergent lineages often results in reduced hybrid viability. Here we report findings from a series of independent molecular analyses over several seasons on four life stages of F1 hybrids between the newts Triturus cristatus and T. marmoratus. These two species form a bimodal hybrid zone of broad overlap in France, with F1 hybrids making up about 4% of the adult population. We demonstrate strong asymmetry in the direction of the cross, with one class (cristatus-mothered) making up about 90% of F1 hybrids. By analyzing embryos and hatchlings, we show that this asymmetry is not due to prezygotic effects, as both classes of hybrid embryos are present at similar frequencies, implicating differential selection on the two hybrid classes after hatching. Adult F1 hybrids show a weak Haldane effect overall, with a 72% excess of females. The rarer marmoratus-mothered class, however, consists entirely of males. The absence of females from this class of adult F1 hybrids is best explained by an incompatibility between the cristatus X chromosome and marmoratus cytoplasm. It is thus important to distinguish the two classes of reciprocal-cross hybrids before making general statements about whether Haldane's rule is observed.
Gene duplication is an evolutionary process in which the emergent property of the whole can become greater and different than the sum of its parts. One potential outcome for gene duplication is for loci to evolve different, yet related functions. In this case, intergenic exchange can shuffle blocks of differentiated nucleotides between paralogues to create new alleles and phenotypes rather than simply homogenize loci. Bioluminescent click beetles in the genus Pyrophorus (Coleoptera: Elateridae) provide an opportunity to explore the creative potential of intergenic exchange for gene family evolution. Pyrophorus beetles bioluminesce different light colors from a pair of dorsal light organs and a ventral light organ. The light organs are under the separate genetic control of dorsal and ventral luciferase loci. Here, we report that intergenic exchange is common between dorsal and ventral loci for beetles from Jamaica (P. plagiophthalamus), the Dominican Republic (P. mellifluous), Belize (P. luscus), and Trinidad (P. noctilucus). We also present evidence that periods of past geographic isolation for beetles on Jamaica, probably acting in concert with selection, built differentiated blocks of substitutions within dorsal and ventral P. plagiophthalamus luciferase loci. Gene flow and intergenic exchange subsequently shuffled these substitutions between dorsal and ventral loci to produce new color phenotypes on Jamaica, including a yellow-green polymorphism. We discuss the possibility of a previously unrecognized emergent evolutionary property of intergenic exchange for luciferase involving cycles of bioluminescent color change related to differences in selective constrains acting on dorsal versus ventral loci. We also explore whether intergenic exchange may commonly create novel variation and the potential for cyclic evolution in other multigene family systems.
Differences in species richness between regions are ultimately explained by patterns of speciation, extinction, and biogeographic dispersal. Yet, few studies have considered the role of all three processes in generating the high biodiversity of tropical regions. A recent study of a speciose group of predominately New World frogs (Hylidae) showed that their low diversity in temperate regions was associated with relatively recent colonization of these regions, rather than latitudinal differences in diversification rates (rates of speciation-extinction). Here, we perform parallel analyses on the most species-rich group of Old World frogs (Ranidae; ∼1300 species) to determine if similar processes drive the latitudinal diversity gradient. We estimate a time-calibrated phytogeny for 390 ranid species and use this phytogeny to analyze patterns of biogeography and diversification rates. As in hylids, we find a strong relationship between the timing of colonization of each region and its current diversity, with recent colonization of temperate regions from tropical regions. Diversification rates are similar in tropical and temperate clades, suggesting that neither accelerated tropical speciation rates nor greater temperate extinction rates explain high tropical diversity in this group. Instead, these results show the importance of historical biogeography in explaining high species richness in both the New World and Old World tropics.
Intercontinental distributions in the southern hemisphere can either be the result of Gondwanan vicariance or more recent transoceanic dispersal. Transoceanic dispersal has come into vogue for explaining many intercontinental distributions; however, it has been used mainly for organisms that can float or raft between the continents. Despite their name, the Sea Catfishes (Ariidae) have limited dispersal ability, and there are no examples of nearshore ariid genera with a transoceanic distribution except for Galeichthys where three species occur in southern Africa and one in the Peruvian coast. A previous study suggested that the group originated in Gondwana, and that the species arrived at their current range after the breakup of the supercontinent in the Early Cretaceous. To test this hypothesis, we infer molecular phylogenies (mitochondrial cytochrome b, ATP synthase 8/6, 12S, and 16S; nuclear rag2; total ∼4 kb) and estimate intercontinental divergence via molecular clocks (penalized-likelihood, Bayesian relaxed clock, and universal clock rates in fishes). Age ranges for cladogenesis of African and South American lineages are 15.4–2.5 my, far more recent than would be suggested by Gondwanan vicariance; thus, the distribution of galeichthyines must be explained by dispersal or more recent vicariant events. The nested position of the Peruvian species (Galeichthys peruvianus) within the African taxa is robust, suggesting that the direction of the dispersal was from Africa to South America. The progenitor of the Peruvian species likely arrived at its current distribution with the aid of ocean currents, and several scenarios are discussed.
Few studies have determined whether formal estimates of selection explain patterns of trait divergence among populations, yet this is one approach for evaluating whether the populations are in equilibria. If adaptive divergence is complete, directional selection should be absent and stabilizing selection should prevail. We estimated natural selection, due to bear predation, acting on the body size and shape of male salmon in three breeding populations that experience differing predation regimes. Our approach was to (1) estimate selection acting within each population on each trait based on an empirical estimate of reproductive activity, (2) test for trait divergence among populations, and (3) test whether selection coefficients were correlated with trait divergence among populations. Stabilizing selection was never significant, indicating that these populations have yet to attain equilibria. Directional selection varied among populations in a manner consistent with trait divergence, indicating ongoing population differentiation. Specifically, the rank order of the creeks in terms of patterns of selection paralleled the rank order in terms of size and shape. The shortest and least deep-bodied males had the highest reproductive activity in the creek with the most intense predation and longer and deeper-bodied males were favored in the creeks with lower predation risk.
The ability of an animal to shed its tail is a widespread antipredator strategy among lizards. The degree of expression of this defense is expected to be shaped by prevailing environmental conditions including local predation pressure. We test these hypotheses by comparing several aspects of caudal autotomy in 15 Mediterranean lizard taxa existing across a swath of mainland and island localities that differ in the number and identity of predator species present. Autotomic ease varied substantially among the study populations, in a pattern that is best explained by the presence of vipers. Neither insularity nor the presence of other types of predators explain the observed autotomy rates. Final concentration of accumulated tail muscle lactate and duration of movement of a shed tail, two traits that were previously thought to relate to predation pressure, are in general not shaped by either predator diversity or insularity. Under conditions of relaxed predation selection, an uncoupling of different aspects of caudal autotomy exists, with some elements (ease of autotomy) declining faster than others (duration of movement, lactate concentration). We compared rates of shed tails in the field against rates of laboratory autotomies conducted under standardized conditions and found very high correlation values (r > 0.96). This suggests that field autotomy rates, rather than being a metric of predatory attacks, merely reflect the innate predisposition of a taxon to shed its tail.
Body size and shape are primary determinants of reproductive output in a variety of taxa, so selection favoring specific body sizes and shapes may, in turn, have a direct affect on reproductive output, and ultimately fitness. In reptiles, species that occupy rocky habitats are often flattened, a morphological character that aids locomotion and life on rocks, but which may constrain reproductive output by reducing the amount of abdominal space available to fill with eggs or offspring. Using 20 species of tropical skink from a wide range of habitats, we quantified habitat use, body height, body volume, and reproductive output, to determine whether the evolution of a flattened body was correlated with a reduction in abdominal volume, and, in turn, with reduced reproductive output. In this group of lizards, the occupation of rocky habitats has led (1) to the evolution of a flattened body, and this shift in body shape has (2) caused a reduction in abdominal volume. Despite this reduction in abdominal volume reproductive output was unaffected, as flatter species compensate by being more “full” of eggs. Thus, we demonstrate that morphological adaptation for enhanced performance in specific habitats did not cause a reduction in instantaneous reproductive output.
The evolution of floral display and flowering time in animal-pollinated plants is commonly attributed to pollinator-mediated selection. Yet, the causes of selection on flowering phenology and traits contributing to floral display have rarely been tested experimentally in natural populations. We quantified phenotypic selection on morphological and phenological characters in the perennial, outcrossing herb Arabidopsis lyrata in two years using female reproductive success as a proxy of fitness. To determine whether selection on floral display and flowering phenology can be attributed to interactions with pollinators, selection was quantified both for open-pollinated controls and for plants receiving supplemental hand-pollination. We documented directional selection for many flowers, large petals, late start of flowering, and early end of flowering. Seed output was pollen-limited in both years and supplemental hand-pollination reduced the magnitude of selection on number of flowers, and reversed the direction of selection on end of flowering. The results demonstrate that interactions with pollinators may affect the strength of selection on floral display and the direction of selection on phenology of flowering in natural plant populations. They thus support the contention that pollinators can drive the evolution of both floral display and flowering time.
Selection is recognized to operate on multiple levels. In disease organisms, selection among hosts is thought to provide an important counterbalance to selection for faster growth within hosts. We performed three experiments, each selecting for a divergence in group size in the entomopathogenic nematode, Steinernema carpocapsae. These nematodes infect and kill insect larvae, reproduce inside the host carcass, and emerge as infective juveniles. We imposed selection on group size by selecting among hosts for either high or low numbers of emerging nematodes. Our goal was to determine whether this trait could respond to selection at the group level, and if so, to examine what other traits would evolve as correlated responses. One of the three experiments showed a significant response to group selection. In that experiment, the high-selected treatment consistently produced more emerging nematodes per host than the low-selected treatment. In addition, nematodes were larger and they emerged later from hosts in the low-selected lines. Despite small effective population sizes, the effects of inbreeding were small in this experiment. Thus, selection among hosts can be effective, leading to both a direct evolutionary response at the population level, as well as to correlated responses in populational and individual traits.
The cichlid fish of Lake Tanganyika in Eastern Africa are a celebrated example of both ecological and species diversification. Because population subdivision is likely to play an important role in the speciation process, understanding how habitat features interact with species' demographic, behavioral and ecological attributes to influence gene flow and population divergence may help explain the causes of high species richness in this and other systems. Here, we test the roles of isolation-by-habitat and isolation-by-distance in generating fine-scale population genetic structure in three sympatric species of habitat-restricted cichlids in Lake Tanganyika. Using multilocus microsatellite genotypes, we contrast patterns of population differentiation in these habitat specialists along a mosaic coastline of both favorable and unfavorable habitat. Despite their close phylogenetic relationship and shared habitat affinity, these species show striking differences in their pattern of genetic subdivision within the same geographical region, suggesting substantially different patterns of gene flow. In particular, two trophically specialized species exhibit much more restricted gene flow over sandy habitat than a trophically opportunistic species. This result suggests that ecological and behavioral traits have a strong influence on the scale and degree of population subdivision, a finding that has potentially important implications for understanding differential propensities for diversification among lineages and phylogenetic patterns of diversity.
The study of mammalian evolution is often based on insights into the evolution of teeth. Developmental studies may attempt to address the mechanisms that guide evolutionary changes. One example is the new developmental model proposed by Kavanagh et al. (2007), which provides a high-level testable model to predict mammalian tooth evolution. It is constructed on an inhibitory cascade model based on a dynamic balance of activators and inhibitors, regulating differences in molar size along the lower dental row. Nevertheless, molar sizes in some mammals differ from this inhibitory cascade model, in particular in voles. The aim of this study is to point out arvicoline and murine differences within this model and to suggest an alternative model. Here we demonstrate that the inhibitory cascade is not followed, due to the arvicoline's greatly elongated first lower molar. We broaden the scope of the macroevolutionary model by projecting a time scale onto the developmental model. We demonstrate that arvicoline evolution is rather characterized by a large gap from the oldest vole to more recent genera, with the rapid acquisition of a large first lower molar contemporaneous to their radiation. Our study provides alternative evolutionary hypotheses for mammals with different trajectories of development.
Given a trade-off between offspring size and number and an advantage to large size in competition, theory predicts that the offspring size that maximizes maternal fitness will vary with the level of competition that offspring experience. Where the strength of competition varies, selection should favor females that can adjust their offspring size to match the offspring's expected competitive environment. We looked for such phenotypically plastic maternal effects in the least killifish, Heterandria formosa, a livebearing, matrotrophic species. Long-term field observations on this species have revealed that some populations experience relatively constant, low densities, whereas other populations experience more variable, higher densities. We compared sizes of offspring born to females exposed during brood development to either low or high experimental densities, keeping the per capita food ration constant. We examined plastic responses to density for females from one population that experiences high and variable densities and another that experiences low and less-variable densities. We found that, as predicted, female H. formosa produced larger offspring at the higher density. Unexpectedly, we found similar patterns of plasticity in response to density for females from both populations, suggesting that this response is evolutionarily conserved in this species.
Finite element (FE) models are popular tools that allow biologists to analyze the biomechanical behavior of complex anatomical structures. However, the expense and time required to create models from specimens has prevented comparative studies from involving large numbers of species. A new method is presented for transforming existing FE models using geometric morphometric methods. Homologous landmark coordinates are digitized on the FE model and on a target specimen into which the FE model is being transformed. These coordinates are used to create a thin-plate spline function and coefficients, which are then applied to every node in the FE model. This function smoothly interpolates the location of points between landmarks, transforming the geometry of the original model to match the target. This new FE model is then used as input in FE analyses. This procedure is demonstrated with turtle shells: a Glyptemys muhlenbergii model is transformed into Clemmys guttata and Actinemys marmorata models. Models are loaded and the resulting stresses are compared. The validity of the models is tested by crushing actual turtle shells in a materials testing machine and comparing those results to predictions from FE models. General guidelines, cautions, and possibilities for this procedure are also presented.
We studied the relative role of genetic determination versus plastic response for traits involved in ecological adaptation of two ecotypes of Littorina saxatilis living at different shore levels. To investigate the magnitude of the plastic response across ontogeny, we compared morphological data from individuals grown in the laboratory and taken from the wild at three developmental stages: shelled embryos, juveniles, and adults. The results indicate that most shell shape variation (72–99%) in adaptive traits (globosity and aperture of the shell) is explained by the ecotype irrespective of the growth environment, suggesting that direct genetic determination is the main factor responsible for the process of adaptation in the wild. There was a tendency for the contribution of plasticity to increase over ontogeny but, in general, the direction of the plastic response did not suggest that this was adaptive.
Interactions between cytoplasmic (generally organelle) and nuclear genomes may be relatively common and could potentially have major fitness consequences. As in the case of within-genome epistasis, this cytonuclear epistasis can favor the evolutionary coadaptation of high-fitness combinations of nuclear and cytoplasmic alleles. Because cytoplasmic factors are generally uniparentally inherited, the cytoplasmic genome is inherited along with only one of the nuclear haplotypes, and therefore, coadaptation is expected to evolve through the interaction of these coinherited (usually maternally inherited) genomes. Here I show that, as a result of this coinheritance of the two genomes, cytonuclear epistasis can favor the evolution of genomic imprinting such that, when the cytoplasmic factor is maternally inherited, selection favors maternal expression of the nuclear locus and when the factor is paternally inherited selection favors paternal expression. Genomic imprinting evolves in this model because it leads to a pattern of gene expression in the nuclear haplotype that is coadapted with (i.e., adaptively coordinated with) gene expression in the coinherited cytoplasmic genome.
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