QUANTITATIVE GENETICS OF BRYOZOAN PHENOTYPIC EVOLUTION. II. ANALYSIS OF SELECTION AND RANDOM CHANGE IN FOSSIL SPECIES USING RECONSTRUCTED GENETIC PARAMETERS

The roles of natural selection and random genetic change in the punctuated phenotypic evolution of eight Miocene-Pliocene tropical American species of the cheilostome bryozoan Metrarabdotos are analyzed by quantitative genetic methods. Trait heritabilities and genetic covariances reconstructed by partitioning within- and among-colony phenotypic variance are similar to those previously obtained for living species of the cheilostome Stylopoma using breeding data. The hypothesis that differences in skeletal morphology between species of Metrarabdotos are entirely due to mutation and genetic drift cannot be rejected for reasonable rates of mutation maintained for periods brief enough to account for the geologically abrupt appearances of these species in the fossil record. Except for one pair of species, separated by the largest morphologic distance, directional selection acting alone would require unrealistically high rates of selective mortality to be maintained for these periods. Thus, directional selection is not strongly implicated in the divergence of Metrarabdotos species. Within species, rates of net phenotypic change are slow enough to require stabilizing selection, but mask large, relatively rapid fluctuations, all of which, however, can be attributed to chance departures from the mean phenotype by mutation and genetic drift, rather than to tracking environmental fluctuation by directional selection. The results are consistent with genetic models involving shifts between multiple adaptive peaks on which phenotypes remain more or less static through long-term stabilizing selection. Regardless of the degree to which directional selection may be involved in peak shifts, phenotypic differentiation is thus related to processes different than the pervasive stabilizing selection acting within species.     

QUANTITATIVE GENETICS OF BRYOZOAN PHENOTYPIC EVOLUTION. III. PHENOTYPIC PLASTICITY AND THE MAINTENANCE OF GENETIC VARIATION

Cheilostome bryozoan species show long-term morphologic stasis, implying stabilizing selection sustained for millions of years, but nevertheless retain significant heritable variation in traits of skeletal morphology. The possible role of within-genotype (within-colony) phenotypic variability in preserving genetic diversity was analyzed using breeding data for two species of Stylopoma from sites along 110 km of the Caribbean coast of Panama. Variation among zooids within colonies accounts for nearly two-thirds of the phenotypic variance on average, increases with environmental heterogeneity, and includes significant genotype-environment interaction. Thus, within-colony variability apparently represents phenotypic plasticity, at least some of which is heritable, rather than random “developmental noise.” Almost all of the among-colonies component of phenotypic variance is accounted for by additive genetic differences in trait means, suggesting that within-colony plasticity includes virtually all of the environmental component of phenotypic variance in these populations of Stylopoma. Thus, heritable within-colony plasticity could play a significant part in maintaining genetic diversity in cheilostomes, but it is also possible that rates of polygenic mutation alone are sufficient to balance the effects of selection.     

QUANTITATIVE GENETICS OF MORPHOLOGICAL DIFFERENTIATION IN PEROMYSCUS. II. ANALYSIS OF SELECTION AND DRIFT

The hypothesis that the morphological divergence of local populations of Peromyscus is due to random genetic drift was evaluated by testing the proportionality of the among-locality covariance matrix, L, and the additive genetic covariance matrix, G. Overall, significant proportionality of L? and ? was not observed, indicating the evolutionary divergence of local populations does not result from random genetic drift. The forces of selection needed to differentiate three taxa of Peromyscus were reconstructed to examine the divergence of species and subspecies. The selection gradients obtained illustrate the inadequacy of univariate analyses of selection by finding that some characters evolve in the direction opposite to the force of selection acting directly on them. A retrospective selection index was constructed using the estimated selection gradients, and truncation selection on this index was used to estimate the minimum selective mortality per generation required to produce the observed change. On any of the time scales used, the proportion of the population that would need to be culled was quite low, the greatest being of the same order of magnitude as the selective intensities observed in extant natural populations. Thus, entirely plausible intensities of directional natural selection can produce species-level differences in a period of time too short to be resolved in the fossil record.     

Population differentiation without speciation

Population differentiation is often viewed as an important step towards speciation, and part of the rationale for conserving variation at the intraspecific level is that the potential to generate more biological diversity should be retained. Yet, speciation is not an inevitable consequence of population divergence. This paper reviews recent work on the Trinidadian guppy, Poecilia reticulata, a species that is renowned for its capacity for population differentiation. Guppy populations evolve rapidly, within 10¹ to 10² generations, as a response to changes in selection exerted by predators. The rates of evolution involved can be up to seven orders of magnitude greater than those seen in the fossil record. Sexual selection, particuarly female choice, appears to reinforce the divergence that natural selection has generated. Perplexingly, however, there is no reproductive isolation (either prezygotic or postzygotic) between populations, even those that have been separated for at least 10⁶ generations. Sexual conflict may be the key to explaining this absence of speciation. Male reproductive behaviour, particularly the high incidence of sneaky mating, may be instrumental in producing sufficient gene flow to prevent reproductive isolation. Sneaky mating has the potential to undermine female choice, and is known to be an important means of sperm transfer in wild populations. Sexual dimorphism, also a result of sexual conflict in guppies, may inhibit speciation in another way. Morphological differences between the sexes, that have arisen for reproductive reasons, mean that males and females are pre-adapted for different foraging niches. This, in turn, reduces the opportunity for the development of feeding polymorphisms, a mechanism that seems to have been important in the sympatric speciation of other fish species.     

Rapid parapatric speciation on holey adaptive landscapes.

A classical view of speciation is that reproductive isolation arises as a by-product of genetic divergence. Here, individual-based simulations are used to evaluate whether the mechanisms implied by this view may result in rapid speciation if the only source of genetic divergence are mutation and random genetic drift. Distinctive features of the simulations are the consideration of the complete process of speciation (from initiation until completion), and of a large number of loci, which was only one order of magnitude smaller than that of bacteria. It is demonstrated that rapid speciation on the time-scale of hundreds of generations is plausible without the need for extreme founder events, complete geographic isolation, the existence of distinct adaptive peaks or selection for local adaptation. The plausibility of speciation is enhanced by population subdivision. Simultaneous emergence of more than two new species from a subdivided population is highly probable. Numerical examples relevant to the theory of centrifugal speciation and to the conjectures about the fate of ''ring species'' and ''sexual continuums'' are presented.     

Local adaptation within a hybrid species

Ecological divergence among populations may be strongly influenced by their genetic background. For instance, genetic admixture through introgressive hybridization or hybrid speciation is likely to affect the genetic variation and evolvability of phenotypic traits. We studied geographic variation in two beak dimensions and three other phenotypic traits of the Italian sparrow (Passer italiae), a young hybrid species formed through interbreeding between house sparrows (P. domesticus) and Spanish sparrows (P. hispaniolensis). We found that beak morphology was strongly influenced by precipitation regimes and that it appeared to be the target of divergent selection within Italian sparrows. Interestingly, however, the degree of parental genetic contribution in the hybrid species had no effect on phenotypic beak variation. Moreover, beak height divergence may mediate genetic differentiation between populations, consistent with isolation-by-adaptation within this hybrid species. The study illustrates how hybrid species may be relatively unconstrained by their admixed genetic background, allowing them to adapt rapidly to environmental variation.     

Phenotypic differentiation is associated with divergent sexual selection among closely related barn swallow populations

Sexual selection plays a key role in the diversification of numerous animal clades and may accelerate trait divergence during speciation. However, much of our understanding of this process comes from phylogenetic comparative studies, which rely on surrogate measures such as dimorphism that may not represent selection in wild populations. In this study, we assess sexual selection pressures for multiple male visual signals across four barn swallow (Hirundo rustica) populations. Our sample encompassed 2400 linear km and two described subspecies: European H. r. rustica (in the Czech Republic and Romania) and eastern Mediterranean H. r. transitiva (in Israel), as well as a potential area of contact (in Turkey). We demonstrate significant phenotypic differentiation in four sexual signalling axes, despite very low‐level genomic divergence and no comparable divergence in an ecological trait. Moreover, the direction of phenotypic divergence is consistent with differences in sexual selection pressures among subspecies. Thus, H. r. transitiva, which have the darkest ventral plumage of any population, experience directional selection for darker plumage. Similarly, H. r. rustica, which have the longest tail feathers of any population, experience directional selection for elongated tail feathers and disruptive selection for ventral plumage saturation. These results suggest that sexual selection is the primary driver of phenotypic differentiation in this species. Our findings add to growing evidence of phenotypic divergence with gene flow. However, to our knowledge, this is the first study to relate direct measures of the strength and targets of sexual selection to phenotypic divergence among closely related wild populations.     

Population genetic structure and a possible role for selection in driving phenotypic divergence in a rainbowfish (Melanotaeniidae)

Quantitative genetic divergence may be driven by drift or selection. The rainbowfish Melanotaenia australis exhibits phenotypic divergence among populations in Western Australia, although the mechanisms driving this divergence are unknown. We used microsatellites to assess neutral genetic divergence (F_ST), and found a hierarchical pattern of subdivision consistent with low divergence between upstream and downstream populations (within drainages), moderate divergence between drainages (within regions), and high divergence between regions. Using a common‐garden approach, we measured quantitative genetic divergence in phenotypic traits (Q_ST). By comparing this to expectations from neutral processes (F_ST), we concluded that the effect of selection varies depending on the spatial scale considered. Within drainages, selection may be causing divergence between upstream and downstream phenotypes but, between regions, selection appears to homogenize phenotypes. This highlights the importance of spatial scale in studies of this kind, and suggests that, because variance in selection pressures can drive speciation, polymorphism in M. australis may represent speciation in action. © 2010 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 144–160.     

Social selection parapatry in Afrotropical sunbirds

The extent of range overlap of incipient and recent species depends on the type and magnitude of phenotypic divergence that separates them, and the consequences of phenotypic divergence on their interactions. Signal divergence by social selection likely initiates many speciation events, but may yield niche‐conserved lineages predisposed to limit each others’ ranges via ecological competition. Here, we examine this neglected aspect of social selection speciation theory in relation to the discovery of a nonecotonal species border between sunbirds. We find that Nectarinia moreaui and Nectarinia fuelleborni meet in a ～6 km wide contact zone, as estimated by molecular cline analysis. These species exploit similar bioclimatic niches, but sing highly divergent learned songs, consistent with divergence by social selection. Cline analyses suggest that within‐species stabilizing social selection on song‐learning predispositions maintains species differences in song despite both hybridization and cultural transmission. We conclude that ecological competition between moreaui and fuelleborni contributes to the stabilization of the species border, but that ecological competition acts in conjunction with reproductive interference. The evolutionary maintenance of learned song differences in a hybrid zone recommend this study system for future studies on the mechanisms of learned song divergence and its role in speciation.     

CALIBRATING DIVERGENCE TIMES ON SPECIES TREES VERSUS GENE TREES: IMPLICATIONS FOR SPECIATION HISTORY OF APHELOCOMA JAYS

Estimates of the timing of divergence are central to testing the underlying causes of speciation. Relaxed molecular clocks and fossil calibration have improved these estimates; however, these advances are implemented in the context of gene trees, which can overestimate divergence times. Here we couple recent innovations for dating speciation events with the analytical power of species trees, where multilocus data are considered in a coalescent context. Divergence times are estimated in the bird genus Aphelocoma to test whether speciation in these jays coincided with mountain uplift or glacial cycles. Gene trees and species trees show general agreement that diversification began in the Miocene amid mountain uplift. However, dates from the multilocus species tree are more recent, occurring predominately in the Pleistocene, consistent with theory that divergence times can be significantly overestimated with gene‐tree based approaches that do not correct for genetic divergence that predates speciation. In addition to coalescent stochasticity, Haldane's rule could account for some differences in timing estimates between mitochondrial DNA and nuclear genes. By incorporating a fossil calibration applied to the species tree, in addition to the process of gene lineage coalescence, the present approach provides a more biologically realistic framework for dating speciation events, and hence for testing the links between diversification and specific biogeographic and geologic events.     

Polygamy slows down population divergence in shorebirds

Sexual selection may act as a promotor of speciation since divergent mate choice and competition for mates can rapidly lead to reproductive isolation. Alternatively, sexual selection may also retard speciation since polygamous individuals can access additional mates by increased breeding dispersal. High breeding dispersal should hence increase gene flow and reduce diversification in polygamous species. Here, we test how polygamy predicts diversification in shorebirds using genetic differentiation and subspecies richness as proxies for population divergence. Examining microsatellite data from 79 populations in 10 plover species (Genus: Charadrius) we found that polygamous species display significantly less genetic structure and weaker isolation‐by‐distance effects than monogamous species. Consistent with this result, a comparative analysis including 136 shorebird species showed significantly fewer subspecies for polygamous than for monogamous species. By contrast, migratory behavior neither predicted genetic differentiation nor subspecies richness. Taken together, our results suggest that dispersal associated with polygamy may facilitate gene flow and limit population divergence. Therefore, intense sexual selection, as occurs in polygamous species, may act as a brake rather than an engine of speciation in shorebirds. We discuss alternative explanations for these results and call for further studies to understand the relationships between sexual selection, dispersal, and diversification.     

Divergence of a speciation trait through artificial selection: Insights into constraints,by-product effects and sexual isolation

Speciation and sexual isolation often occur when divergent female mating preferences target male secondary sexual traits. Despite the importance of such male signals, little is known about their evolvability and genetic linkage to other traits during speciation. To answer these questions, we imposed divergent artificial selection for 10 non-overlapping generations on the Inter-Pulse-Interval (IPI) of male courtship songs; which has been previously shown to be a major species recognition trait for females in the Drosophila athabasca species complex. Focusing on one of the species, Drosophila mahican (previously known as EA race), we examined IPI's: (1) rate of divergence, (2) response to selection in different directions, (3) genetic architecture of divergence and (4) by-product effects on other traits that have diverged in the species complex. We found rapid and consistent response for higher IPI but less response to lower IPI; implying asymmetrical constraints. Genetic divergence in IPI differed from natural species in X versus autosome contribution and in dominance, suggesting that evolution may take different paths. Finally, selection on IPI did not alter other components of male songs, or other ecological traits, and did not cause divergence in female preferences, as evidenced by lack of sexual isolation. This suggests that divergence of male courtship song IPI is unconstrained by genetic linkage with other traits in this system. This lack of linkage between male signals and other traits implies that female preferences or ecological selection can co-opt and mould specific male signals for species recognition free of genetic constraints from other traits.     

MUTATION LOAD AND THE SURVIVAL OF SMALL POPULATIONS

Previous attempts to model the joint action of selection and mutation in finite populations have treated population size as being independent of the mutation load. However, the accumulation of deleterious mutations is expected to cause a gradual reduction in population size. Consequently, in small populations random genetic drift will progressively overpower selection making it easier to fix future mutations. This synergistic interaction, which we refer to as a mutational melt-down, ultimately leads to population extinction. For many conditions, the coefficient of variation of extinction time is less than 0.1, and for species that reproduce by binary fission, the expected extinction time is quite insensitive to population carrying capacity. These results are consistent with observations that many cultures of ciliated protozoans and vertebrate fibroblasts have characteristic extinction times. The model also predicts that clonal lineages are unlikely to survive more than 10⁴ to 10⁵ generations, which is consistent with existing data on parthenogenetic animals. Contrary to the usual view that Muller's ratchet does more damage when selection is weak, we show that the mean extinction time declines as mutations become more deleterious. Although very small sexual populations, such as self-fertilized lines, are subject to mutational meltdowns, recombination effectively eliminates the process when the effective population size exceeds a dozen or so. The concept of the effective mutation load is developed, and several procedures for estimating it are described. It is shown that this load can be reduced substantially when mutational effects are highly variable.     

QTL analysis of a rapidly evolving speciation phenotype in the Hawaiian cricket Laupala

In mate recognition systems, the functional necessity to coordinate traits involved in sexual communication should result in reduced pairing potential for new variants outside the distribution of common reproductive signals. Yet, many closely related, sexual species differ in mate recognition traits, suggesting that directional selection influences the divergence of mate recognition systems. Species of the endemic Hawaiian cricket genus Laupala are morphologically and ecologically cryptic, although both male calling song and female acoustic preference have diverged rapidly between closely related species. These mate recognition phenotypes are therefore often likely to be speciation phenotypes, i.e. traits whose divergence contributes, directly or indirectly, to a reduction of gene flow during speciation, given their frequent participation in early lineage divergence. We conducted a replicated, quantitative trait loci (QTL) mapping study of the genetic basis of differences in male calling song between two closely related species, Laupala paranigra and Laupala kohalensis, allowing us to examine the genetic basis of traits involved in rapid speciation. We found statistical support for eight QTL in one replicate, with at least four of these QTL mapping to the same regions in a second replicate. QTL effects ranged between 3.0% and 10.7% of the difference in pulse rate between L. paranigra and L. kohalensis, and are thus of moderate to small effect. All QTL identified show directional effects consistent with the hypothesis of directional selection. Thus, we conclude that rapid speciation can occur under the influence of many genes of moderate to small effect. This study implicates the role of directional selection in the divergence of mate recognition traits and speciation the Hawaiian cricket genus Laupala.     

THE EVOLUTION OF RESISTANCE TO HERBIVORY IN IPOMOEA PURPUREA. I. ATTEMPTS TO DETECT SELECTION

In this study, we looked for evidence of directional or stabilizing/disruptive selection on plant size and on the level of damage (resistance) caused by four types of herbivores in the annual morning glory Ipomoea purpurea. Selection was estimated by standard phenotypic regression analysis and by regression on breeding values. The phenotypic regression analysis revealed directional selection for all five characters (i.e., plant size and resistance to four types of herbivores) and indicated that plant size and resistance to corn-earworm damage were subject to stabilizing selection. By contrast, the analysis using breeding values revealed directional selection only for plant size and resistance to corn earworms, while none of the characters examined indicated stabilizing or disruptive selection. These results suggest that intermediate levels of damage in I. purpurea are, in general, not maintained by stabilizing selection. Rather, they may reflect either 1) a transient state that exists while directional selection pushes the population toward complete resistance (or, in one case, total absence of resistance) or 2) the evolution of susceptibility to damage by genetic drift.     

Mutation‐order divergence by sexual selection: diversification of sexual signals in similar environments as a first step in speciation

The origin of species remains a central question, and recent research focuses on the role of ecological differences in promoting speciation. Ecological differences create opportunities for divergent selection (i.e. ‘ecological’ speciation), a Darwinian hypothesis that hardly requires justification. In contrast, ‘mutation‐order’ speciation proposes that, instead of adapting to different environments, populations find different ways to adapt to similar environments, implying that speciation does not require ecological differences. This distinction is critical as it provides an alternative hypothesis to the prevailing view that ecological differences drive speciation. Speciation by sexual selection lies at the centre of debates about the importance of ecological differences in promoting speciation; here, we present verbal and mathematical models of mutation‐order divergence by sexual selection. We develop three general cases and provide a two‐locus population genetic model for each. Results indicate that alternative secondary sexual traits can fix in populations that initially experience similar natural and sexual selection and that divergent traits and preferences can remain stable in the face of low gene flow. This stable divergence can facilitate subsequent divergence that completes or reinforces speciation. We argue that a mutation‐order process could explain widespread diversity in secondary sexual traits among closely related, allopatric species.     

Divergent selection and phenotypic plasticity during incipient speciation in Lake Victoria cichlid fish

Divergent selection acting on several different traits that cause multidimensional shifts are supposed to promote speciation, but the outcome of this process is highly dependent on the balance between the strength of selection vs. gene flow. Here, we studied a pair of sister species of Lake Victoria cichlids at a location where they hybridize and tested the hypothesis that divergent selection acting on several traits can maintain phenotypic differentiation despite gene flow. To explore the possible role of selection we tested for correlations between phenotypes and environment and compared phenotypic divergence (P_ST) with that based on neutral markers (F_ST). We found indications for disruptive selection acting on male breeding colour and divergent selection acting on several morphological traits. By performing common garden experiments we also separated the environmental and heritable components of divergence and found evidence for phenotypic plasticity in some morphological traits contributing to species differences.     

Natural selection on the genetical component of variance in body condition in a wild bird population

Although there is substantial evidence that skeletal measures of body size are heritable in wild animal populations, it is frequently assumed that the nonskeletal component of body weight (or ‘condition’) is determined primarily by environmental factors, in particular nutritional state. We tested this assumption by quantifying the genetic and environmental components of variance in fledgling body condition index (=relative body weight) in a natural population of collared flycatchers (Ficedula albicollis), and compared the strength of natural selection on individual breeding values with that on phenotypic values. A mixed model analysis of the components of variance, based on an ‘animal model’ and using 18 years of data on 17 717 nestlings, revealed a significant additive genetic component of variance in body condition, which corresponded to a narrow sense heritability (h²) of 0.30 (SE=0.03). Nongenetic contributions to variation in body condition were large, but there was no evidence of dominance variance nor of contributions from early maternal or common environment effects (pre‐manipulation environment) in condition at fledging. Comparison of pre‐ and post‐selection samples revealed virtually identical h² of body condition index, despite the fact that there was a significant decrease (35%) in the levels of additive genetic variance from fledging to breeding. The similar h² in the two samples occurred because the environmental component of variance was also reduced by selection, suggesting that natural selection was acting on both genotypic and environmental variation. The effects of selection on genetic variance were confirmed by calculation of the selection differentials for both phenotypic values and best linear unbiased predictor (BLUP) estimates of breeding values: there was positive directional selection on condition index both at the phenotypic and the genotypic level. The significant h² of body condition index is consistent with data from human and rodent populations showing significant additive genetic variance in relative body mass and adiposity, but contrasts with the common assumption in ecology that body condition reflects an individual’s nongenetic nutritional state. Furthermore, the substantial reduction in the additive genetic component of variance in body condition index suggests that selection on environmental deviations cannot alone explain the maintenance of additive genetic variation in heritable traits, but that other mechanisms are needed to explain the moderate to high heritabilities of traits under consistent and strong directional selection.     

Patterns of parapatric speciation

Abstract. Geographic variation may ultimately lead to the splitting of a subdivided population into reproductively isolated units in spite of migration. Here, we consider how the waiting time until the first split and its location depend on different evolutionary factors including mutation, migration, random genetic drift, genetic architecture, and the geometric structure of the habitat. We perform large-scale, individual-based simulations using a simple model of reproductive isolation based on a classical view that reproductive isolation evolves as a by-product of genetic divergence. We show that rapid parapatric speciation on the time scale of a few hundred to a few thousand generations is plausible even when neighboring subpopulations exchange several individuals each generation. Divergent selection for local adaptation is not required for rapid speciation. Our results substantiates the claims that species with smaller range sizes (which are characterized by smaller local densities and reduced dispersal ability) should have higher speciation rates. If mutation rate is small, local abundances are low, or substantial genetic changes are required for reproductive isolation, then central populations should be the place where most splits take place. With high mutation rates, high local densities, or with moderate genetic changes sufficient for reproductive isolation, speciation events are expected to involve mainly peripheral populations.     

Persistence in peripheral refugia promotes phenotypic divergence and speciation in a rainforest frog

It is well established from the fossil record and phylogeographic analyses that late Quaternary climate fluctuations led to substantial changes in species' distribution, but whether and how these fluctuations resulted in phenotypic divergence and speciation is less clear. This question can be addressed through detailed analysis of traits relevant to ecology and mating within and among intraspecific lineages that persisted in separate refugia. In a biogeographic system (the Australian Wet Tropics [AWT]) with a well-established history of refugial isolation during Pleistocene glacial periods, we tested whether climate-mediated changes in distribution drove genetic and phenotypic divergence in the rainforest frog Cophixalus ornatus. We combined paleomodeling and multilocus genetics to demonstrate long-term persistence within, and isolation among, one central and two peripheral refugia. In contrast to other AWT vertebrates, the three major lineages differ in ecologically relevant morphology and in mating call, reflecting divergent selection and/or genetic drift in the peripheral isolates. Divergence in mating call and contact zone analyses suggest that the lineages now represent distinct species. The results show that climate shifts can promote genetic and phenotypic divergence and, potentially, speciation and direct attention toward incorporating adaptive traits into phylogeographic studies to better resolve the mechanisms of speciation.