It is widely accepted that bigger entities have a greater division of labor than smaller ones and this is reflected in the fact that larger multicellular organisms have a corresponding increase in the number of their cell types. This rule is examined in some detail from very small organisms to large animals, and plants, and societies. Compared to other size-related rules, the size-complexity rule is relatively rough and approximate, yet clearly it holds throughout the whole range of living organisms, as well as for societies. The relationship between size and complexity is analyzed by examining the effects of size increase and decrease: size increase requires an increase in complexity, whereas size decrease permits, and sometimes requires, a decrease in complexity. Conversely, an increase or decrease in complexity permits, but does not require changes in size. An especially compelling argument for the close relation between size and complexity can be found in size quorum sensing in very small multicellular organisms.

It has been proposed that effective size could be estimated in small dioecious population by considering the heterozygote excess observed at neutral markers. When the number of breeders is small, allelic frequencies in males and females will slightly differ due to binomial sampling error. However, this excess of heterozygotes is not generated by dioecy but by the absence of individuals produced through selfing. Consequently, the approach can also be applied to self-incompatible monoecious species. Some inaccuracies in earlier equations expressing effective size as function of the heterozygote excess are also corrected in this paper. The approach is then extended to subdivided populations, where time of sampling becomes crucial. When adults are sampled, the effective size of the entire population can be estimated, whereas when juveniles are sampled, the average effective number of breeders per subpopulations can be estimated. The main limitation of the heterozygote excess method is that it will only perform satisfactorily for populations with a small number of reproducing individuals. While this situation is unlikely to happen frequently at the scale of the entire population, structured populations with small subpopulations are likely to be common. The estimation of the average number of breeders per subpopulations is thus expected to be applicable to many natural populations. The approach is straightforward to compute and independent of equilibrium assumptions. Applications to simulated data suggest the estimation of the number of breeders to be robust to mutation and migration rates, and to specificities of the mating system.

Cytoplasmic incompatibility (CI) is induced in arthropods by the maternally inherited bacterium Wolbachia. When infected males mate with uninfected females or with females bearing a different Wolbachia variant, paternal chromosomes behave abnormally and embryos die. This pattern can be interpreted as resulting from two bacterial effects: One (usually termed mod, for modification) would affect sperm and induce embryo death, unless Wolbachia is also present in the egg, which implies the existence of a second effect, usually termed resc, for rescue. The fact that CI can occur in crosses between males and females infected by different Wolbachia shows that mod and resc interact in a specific manner. In other words, different compatibility types, or mod/resc pairs seem to have diverged from one (or a few) common ancestor(s). We are interested in the process allowing the evolution of mod/resc pairs. Here this question is addressed experimentally after cytoplasmic injection into a single host species (Drosophila simulans) by investigating compatibility relationships between closely related Wolbachia variants naturally evolving in different dipteran hosts: D. simulans, Drosophila melanogaster, and Rhagoletis cerasi. Our results suggest that closely related bacteria can be totally or partially incompatible. The compatibility relationships observed can be explained using a formal description of the mod and resc functions, implying both qualitative and quantitative variations.

Plant-fungal symbioses include many familiar antagonistic and mutualistic associations and some model cases of coevolution. The relationship between coevolution at the different evolutionary scales has remained an open question. Widespread host specificity and documented host switches offer conflicting indications of what to expect from comparisons of plant and fungal phylogenies. This study sought to establish the role of plant phylogeny in determining fungal phylogeny and the relative contributions of codivergence and host switching by comparing tree topologies for 15 plant-fungal symbioses. Second it attempted to characterize the relationship between phylogenetic congruence and switching. Trees were estimated from published sequences and reconciliation analysis was applied in the form of cophylogeny mapping using “jungles”. This provided an exhaustive account of all possible switches capable of reconciling two associated phylogenies. A continuum of cophylogenetic dynamics was identified, ranging from mostly codivergence (e.g., Exobasidium) to mostly switching, (e.g., Erysiphe). Surprisingly, congruent solutions do not necessarily have fewer switches when using cophylogeny mapping, but a significant negative relationship between congruence and the distance of switches proved to be a useful indicator. According to reconciliation analysis, the contribution of host phylogeny varies widely across plant-fungal symbioses, making host specificity and coadaptation poor indicators of macroevolutionary trends because they are necessary, but not sufficient, conditions.

Pollen limitation affects plants with diverse reproductive systems and ecologies. In self-incompatible (SI) species, pollen limitation may preclude full reproductive compensation for prezygotic rejection of pollen. We present a model designed to explore the effects of incomplete reproductive compensation on evolutionary changes at a modifier locus that regulates the level of SI expression. Our results indicate that incomplete reproductive compensation greatly increases the evolutionary costs of SI, particularly in populations with low S-allele diversity. The evolutionary fate of modifiers of SI expression depends on the rate at which they are transmitted to future generations as well as the effects of SI on offspring number and quality. Partial SI expression can represent a stable condition rather than an evolutionarily transient state between full expression and full suppression. This unanticipated result provides the first theoretical support for the evolutionary stability of such mixed mating systems, the existence of which has recently been documented.

Sexual dimorphism is one of the most widespread and recognizable patterns of phenotypic variation in the biotic world. Sexual dimorphism in floral display is striking in the dioecious plant Silene latifolia, with males making many, small flowers compared to females. We investigated this dimorphism via artificial selection on two populations to determine whether genetic variation exists within populations for flower size and the extent of the between-sex correlation, whether a flower size and number trade-off exists within each sex, and whether pollen and ovule production vary with flower size. We selected for decreased flower size (calyx width) in females and increased flower size in males and measured the response to selection in size and correlated responses in flower dry mass, flower number, and pollen or ovule number per flower. Four bouts of selection in each of two selection programs were performed, for a total of three selection lines to decrease size, three to increase it, and two control lines. Flower size always significantly responded to selection and we always found a significant correlated response in the sex not under selection. Selection decreased but did not eliminate the sexual dimorphism in flower dry mass and number. A negative relationship between flower size and number within each sex was revealed. Whereas ovule number showed a significant correlated response to selection on flower size, pollen number did not. Our results indicate that although substantial additive genetic variation for flower size exists, the high between-sex genetic correlation would likely constrain flower size from becoming more sexually dimorphic. Furthermore, floral display within each sex is constrained by a flower size and number trade-off. Given this trade-off and lack of variation in pollen production with flower size, we suggest that sexual dimorphism evolved via sexual selection to increase flower number in males but not females.

Male structures specialized to contact females during sexual interactions often diverge relatively rapidly over evolutionary time. Previous explanations for this pattern invoked sexual selection by female choice, but new ideas emphasize possible sexually antagonistic coevolution resulting from male-female conflict over control of fertilization. The two types of selection have often not been carefully distinguished. They do not theoretically exclude one another, but they have not necessarily had equally important roles in producing rapid evolutionary divergence. To date, most recent empirical studies of antagonistic coevolution have emphasized only a few taxa. This study uses the abundant but little-used data in the taxonomic literature on morphology to evaluate the roles of antagonistic coevolution and traditional female choice over a wide taxonomic spectrum (61 families of arthropods, mostly insects and spiders). Groups with species-specific male structures that contact females were checked for coevolution of species-specific female structures that are contacted by the male and that have mechanical properties that could potentially defend her against the male. Facultatively deployable, species-specific female defensive structures, a design that would seem likely to evolve frequently under the sexually antagonistic coevolution hypothesis, were completely absent (0% of 106 structures in 84 taxonomic groups). Although likely cases of sexually antagonistic coevolution exist, using conservative criteria, 79.2% of the 106 structures lacked even potentially defensive female coevolution. A common pattern (53.8% of 106) was a nearly complete absence of female change in areas contacted by species-specific male structures. Post-hoc arguments invoking possible coevolution of defensive female behavior instead of morphology, or of female sensitivities and responses to male sensory traps, could enable the sexually antagonistic coevolution hypothesis to explain these data. No case of such coevolution of female behavior or sensitivities has been demonstrated, and there are additional reasons to doubt that they are general explanations for the data presented here. Detailed studies of female resistance behavior could help illuminate several issues. The possibility of a greater role for antagonistic coevolution in reproductive physiology than in morphology and the possibility that female choice and sexually antagonistic coevolution have both been important in some lineages are discussed.

Comparisons between closely related species in different habitats provide a window into understanding how biotic factors shape evolutionary pathways. Weevils in the genus Curculio have radiated extensively across the Palearctic, where similar ecomorphs have evolved independently on different hosts. We examined ecological and morphological data for 31 Curculio species using multivariate statistics to determine which morphological traits covary and which correlate with the host seed size. A subset of 15 taxa for which phylogenetic relationships were known were used for comparative analyses and inferring historical patterns of trait evolution. The morphological analyses suggest rostrum size increased proportionately to body size in both males and females and that both rostrum and body size correlate with host seed size but that rostrum shape does not correlate with any of the seed traits used in the analyses. Host shifts from small seeds to considerably larger seeds or vice versa have occurred several times independently and historical trait evolution indicates that these host shifts were accompanied by morphological changes in rostrum size. These patterns suggest that seed size is an important selective agent for changes in rostrum length along with body size and thus may be a key factor promoting morphological differentiation in the genus Curculio.

Herbivorous insects and other small consumers are often specialized both in use of particular host taxa and in use of particular host tissues. Such consumers also often seem to show consistent differences in the rates of evolution of these two dimensions of host use, implying common processes, but this has been little studied. Here we quantify these rates of change in host use evolution in a major radiation of herbivorous insects, the Chrysomeloidea, whose diversity has been attributed to their use of flowering plants. We find a significant difference in the rates of evolutionary change in these two dimensions of host use, with host taxon associations most labile. There are apparently similar differences in rates of host use evolution in other parasite groups, suggesting the generality of this pattern. Divergences in parasite form associated with use of different host tissues may facilitate resource partitioning among successive adaptive radiations on particular host taxa.

Maternal inputs to offspring early in development are initially high but the process of development suggests that ontogenetic shifts in the importance of maternal genetic variation relative to other sources should occur. We investigated additive genetic variance and covariance for direct (animal), sire, and maternal effects on embryonic length (EL), yolk sac volume (YSV), and alevin (after yolk sac resorption) length (AL) for 460 embryonic and 460 alevin brook charr (Salvelinus fontinalis) in 23 half-sib families (12 sires, 23 dams). There were no additive genetic effects of sires or individual animals on their own phenotype using sire-dam and maternal-animal models for YSV or EL (h²_a < 0.05). However, at the alevin stage we detected low but significant heritability for AL (h²_a = 0.14 ± 0.11). Conversely, maternal genetic effects were high for both embryonic traits (h²_EL = 0.61 ± 0.05; h²_YSV = 0.57 ± 0.06) but faded rapidly for postresorption length (h²_AL = 0.18 ± 0.04). Maternal effects in the sire-dam model corresponded highly with those in the animal-dam model. We did not detect significant genetic covariance between progeny and dams for preresorption traits or between sires and dams for any trait. However, following resorption of the yolk sac, the genetic value of dams for AL was negatively correlated with that of individual progeny (r_m,a = −0.38 ± 0.13), suggesting trade-offs and/or stabilizing selection between maternal and animal genetic trait value. This finding was supported by models of dam fecundity on offspring length and dam weight in phenotypic space. Heritability estimates using simple regression of embryo phenotype on adult parental phenotype produced upwardly biased estimates of genetic variance (h² > 1.0). We propose that development through the embryo-alevin boundary may be a major point in salmonids for ontogenetic changes in the genetic architecture of embryo size from maternal genetic effects to those of the individual organism, and that maternal-offspring conflicts in resource allocation related to size may be partially indicated by negative genetic covariance.

The additive genetic variance-covariance matrix (G) is a concept central to discussions about evolutionary change over time in a suite of traits. However, at the moment we do not know how fast G itself changes as a consequence of selection or how sensitive it is to environmental influences. We investigated possible evolutionary divergence and environmental influences on G using data from a factorial common-garden experiment where common frog (Rana temporaria) tadpoles from two divergent populations were exposed to three different environmental treatments. G-matrices were estimated using an animal model approach applied to data from a NCII breeding design. Matrix comparisons using both Flury and multivariate analysis of variance methods revealed significant differences in G matrices both between populations and between treatments within populations, the former being generally larger than the latter. Comparison of levels of population differentiation in trait means using Q_ST indices with that observed in microsatellite markers (F_ST) revealed that the former values generally exceeded the neutral expectation set by F_ST. Hence, the results suggest that intraspecific divergence in G matrix structure has occurred mainly due to natural selection.

Inferring the spatial expansion dynamics of invading species from molecular data is notoriously difficult due to the complexity of the processes involved. For these demographic scenarios, genetic data obtained from highly variable markers may be profitably combined with specific sampling schemes and information from other sources using a Bayesian approach. The geographic range of the introduced toad Bufo marinus is still expanding in eastern and northern Australia, in each case from isolates established around 1960. A large amount of demographic and historical information is available on both expansion areas. In each area, samples were collected along a transect representing populations of different ages and genotyped at 10 microsatellite loci. Five demographic models of expansion, differing in the dispersal pattern for migrants and founders and in the number of founders, were considered. Because the demographic history is complex, we used an approximate Bayesian method, based on a rejection-regression algorithm, to formally test the relative likelihoods of the five models of expansion and to infer demographic parameters. A stepwise migration-foundation model with founder events was statistically better supported than other four models in both expansion areas. Posterior distributions supported different dynamics of expansion in the studied areas. Populations in the eastern expansion area have a lower stable effective population size and have been founded by a smaller number of individuals than those in the northern expansion area. Once demographically stabilized, populations exchange a substantial number of effective migrants per generation in both expansion areas, and such exchanges are larger in northern than in eastern Australia. The effective number of migrants appears to be considerably lower than that of founders in both expansion areas. We found our inferences to be relatively robust to various assumptions on marker, demographic, and historical features. The method presented here is the only robust, model-based method available so far, which allows inferring complex population dynamics over a short time scale. It also provides the basis for investigating the interplay between population dynamics, drift, and selection in invasive species.

The deleterious effects of inbreeding can be substantial in wild populations and mechanisms to avoid such matings have evolved in many organisms. In situations where social mate choice is restricted, extrapair paternity may be a strategy used by females to avoid inbreeding and increase offspring heterozygosity. In the cooperatively breeding Seychelles warbler, Acrocephalus sechellensis, neither social nor extrapair mate choice was used to avoid inbreeding facultatively, and close inbreeding occurred in approximately 5% of matings. However, a higher frequency of extragroup paternity may be selected for in female subordinates because this did reduce the frequency of mating between close relatives. Inbreeding resulted in reduced individual heterozygosity, which, against expectation, had an almost significant (P = 0.052), positive effect on survival. Conversely, low heterozygosity in the genetic mother was linked to reduced offspring survival, and the magnitude of this intergenerational inbreeding depression effect was environment-dependent. Because we controlled for genetic effects and most environmental effects (through the experimental cross-fostering of nestlings), we conclude that the reduced survival was a result of maternal effects. Our results show that inbreeding can have complicated effects even within a genetic bottlenecked population where the “purging” of recessive alleles is expected to reduce the effects of inbreeding depression.

The songs of many birds are unusual in that they serve a role in identifying conspecific mates, yet they are also culturally transmitted. Noting the apparently high rate of diversity in one avian taxon, the songbirds, in which song learning appears ubiquitous, it has often been speculated that cultural transmission may increase the rate of speciation. Here we examine the possibility that song learning affects the rate of allopatric speciation. We construct a population-genetic model of allopatric divergence that explores the evolution of genes that underlie learning preferences (predispositions to learn some songs over others). We compare this with a model in which mating signals are inherited only genetically. Models are constructed for the cases where songs and preferences are affected by the same or different loci, and we analyze them using analytical local stability analysis combined with simulations of drift and directional sexual selection. Under nearly all conditions examined, song divergence occurs more readily in the learning model than in the nonlearning model. This is a result of reduced frequency-dependent selection in the learning models. Cultural evolution causes males with unusual genotypes to tend to learn from the majority of males around them, and thus develop songs compatible with the majority of the females in the population. Unusual genotypes can therefore be masked by learning. Over a wide range of conditions, learning therefore reduces the waiting time for speciation to occur and can be predicted to accelerate the rate of speciation.

A complete understanding of the speciation process requires the identification of genomic regions and genes that confer reproductive barriers between species. Empirical and theoretical research has revealed two important patterns in the evolution of reproductive isolation in animals: isolation typically arises as a result of disrupted epistatic interactions between multiple loci and these disruptions map disproportionately to the X chromosome. These patterns suggest that a targeted examination of natural gene flow between closely related species at X-linked markers with known positions would provide insight into the genetic basis of speciation. We take advantage of the existence of genomic data and a well-documented European zone of hybridization between two species of house mice, Mus domesticus and M. musculus, to conduct such a survey. We evaluate patterns of introgression across the hybrid zone for 13 diagnostic X-linked loci with known chromosomal positions using a maximum likelihood model. Interlocus comparisons clearly identify one locus with reduced introgression across the center of the hybrid zone, pinpointing a candidate region for reproductive isolation. Results also reveal one locus with high frequencies of M. domesticus alleles in populations on the M. musculus side of the zone, suggesting the possibility that positive selection may act to drive the spread of alleles from one species on to the genomic background of the other species. Finally, cline width and cline center are strongly positively correlated across the X chromosome, indicating that gene flow of the X chromosome may be asymmetrical. This study highlights the utility of natural populations of hybrids for mapping speciation genes and suggests that the middle of the X chromosome may be important for reproductive isolation between species of house mice.

The evolution of behavior has been notoriously difficult to study at the molecular level, but mouse genetic technology offers new promise. We applied selective breeding to increase voluntary wheel running in four replicate lines of Mus domesticus (S mice) while maintaining four additional lines through random breeding to serve as controls (C mice). The goal of the study was to identify the gene expression profile of the hippocampus that may have evolved to facilitate the increased voluntary running. The hippocampus was of interest because it is known to display marked physiological responses in association with wheel running itself. We used high-density oligonucleotide arrays representing 11,904 genes. To control for the confounding influence of physical activity itself on gene expression, animals were housed individually without access to running wheels, and were sampled during the day when they are normally inactive. Two-month-old female mice in estrus were used (n = 16 total; two per line; 8 S and 8 C). After correcting for an acceptable false discovery rate (10%), 30 genes, primarily involved in transcription and translation, significantly increased expression whereas 23 genes, distributed among many categories including immune function and neuronal signaling, decreased expression in S versus C mice. These changes were relatively small in magnitude relative to the changes in gene expression that occur in the hippocampus in response to wheel running itself. A priori tests of dopamine receptor expression levels demonstrated an increase of approximately 20% in the expression of D2 and D4 receptors. These results suggest that relatively small changes in the expression patterns of hippocampal genes underlie large changes in phenotypic response to selection, and that the genetic architecture of running motivation likely involves the dopaminergic system as well as CNS signaling machinery.

Recent genetic studies of natural populations have shown that heterozygosity and other genetic estimates of parental relatedness correlate with a wide variety of fitness traits, from juvenile survival and parasite resistance to male reproductive success. Many of these traits involve health and survival, where the underlying mechanism may involve changes in the effectiveness of the immune system. However, for traits such as reproductive success, the likely mechanisms remain less obvious. In this paper, we examine the relationship between heterozygosity and a range of traits that contribute to male reproductive success, including time spent on territories and competitiveness. Our analysis is based on observational and genetic data from eight consecutive breeding seasons at a colony of the Antarctic fur seal, Arctocephalus gazella. Overall, male reproductive success was found to correlate strongly with internal relatedness (IR, a form of heterozygosity). When different components of success were analyzed, we found that IR correlates independently with reproductive longevity, time spent ashore, and competitive ability per unit mating opportunity on the study beach, with more heterozygous males being more successful. Behavioral observations were sufficiently detailed to allow examination of how daily mean IR values for males present on the beach varied within seasons and from year to year. Again, significant variation was found both among and within seasons, with more homozygous males appearing less able to hold territories in poor seasons when pup production is low and, within a season, at both the start of the season and to some extent around the peak of female estrus. Finally, we tested whether the benefits of high heterozygosity are due mainly to a genomewide effect (e.g. inbreeding depression) or to single locus heterosis by asking whether the relationship between IR and male success was robust to the removal of any single locus or to any pair of loci. Since the relationship remained significant in all cases, we favor a multilocus explanation for the effects we report.

Understanding the genetic basis to landscape vegetation structure is an important step that will allow us to examine ecological and evolutionary processes at multiple spatial scales. Here for the first time we show that the fractal architecture of a dominant plant on the landscape exhibits high broad-sense heritability and thus has a genetic basis. The fractal architecture of trees is known to influence ecological communities associated with them. In a unidirectional cottonwood-hybridizing complex (Populus angustifolia × P. fremontii) pure and hybrid cottonwoods differed significantly in their fractal architecture, with phenotypic variance among backcross hybrids exceeding that of F₁ hybrids and of pure narrowleaf cottonwoods by two-fold. This result provides a crucial link between genes and fractal scaling theory, and places the study of landscape ecology within an evolutionary framework.

Employing an integrative approach to investigate the evolution of morphology can yield novel perspectives not attainable from a single field of study. Studies of limb loss and body elongation in squamates (snakes and lizards) present a good example in which integrating studies of systematics and ecology with genetics and development can provide considerable new insight. In this comment we address several misunderstandings of the developmental genetic literature presented in a paper by Wiens and Slingluff (2001) to counter their criticism of previous work in these disciplines and to clarify the apparently contradictory data from different fields of study. Specifically, we comment on (1) the developmental mechanisms underlying axial regionalization, body elongation, and limb loss; (2) the utility of presacral vertebral counts versus more specific partitioning of the primary body axis; (3) the independent, modular nature of limbs and limb girdles and their utility in diagnosing genetic changes in development; and (4) the causal bases of hind limb reduction in ophidian and nonophidian squamates.