Pim Edelaar

On the Origin of Species by Natural and Sexual Selection

Local Selection of Magic Traits Ecological interactions can favor specialization, and sexual selection can induce reproductive isolation; however, these processes are insufficient by themselves to create new species. They must act in concert and on the same set of genes. Van Doorn et al. (p. 1704, published online 26 November; see the Perspective by Mank) present a theoretical model that shows that within a larger population the evolution of mating preferences will favor sexual ornaments that indicate the degree of adaptation to the local ecological conditions, for example, the abundant song of a male bird that can obtain food easily because it has the right bill size for the seeds in that locale. Once mate choice evolves on the basis of a signal of local adaptation, natural and sexual selection will mutually enforce each other, ultimately leading to speciation. Modeling demonstrates how speciation occurs due to sexual selection. Ecological speciation is considered an adaptive response to selection for local adaptation. However, besides suitable ecological conditions, the process requires assortative mating to protect the nascent species from homogenization by gene flow. By means of a simple model, we demonstrate that disruptive ecological selection favors the evolution of sexual preferences for ornaments that signal local adaptation. Such preferences induce assortative mating with respect to ecological characters and enhance the strength of disruptive selection. Natural and sexual selection thus work in concert to achieve local adaptation and reproductive isolation, even in the presence of substantial gene flow. The resulting speciation process ensues without the divergence of mating preferences, avoiding problems that have plagued previous models of speciation by sexual selection.

MATCHING HABITAT CHOICE CAUSES DIRECTED GENE FLOW: A NEGLECTED DIMENSION IN EVOLUTION AND ECOLOGY

Abstract Gene flow among populations is typically thought to be antagonistic to population differentiation and local adaptation. However, this assumes that dispersing individuals disperse randomly with respect to their ability to use the environment. Yet dispersing individuals often sample and compare environments and settle in those environments that best match their phenotype, causing directed gene flow, which can in fact promote population differentiation and adaptation. We refer to this process as “matching habitat choice.” Although this process has been acknowledged by several researchers, no synthesis or perspective on its potentially widespread importance exists. Here we synthesize empirical and theoretical studies, and offer a new perspective that matching habitat choice can have significant effects on important and controversial topics. We discuss the potential implications of matching habitat choice for the degree and rate of local adaptation, the evolution of niche width, adaptive peak shifts, speciation in the presence of gene flow, and on our view and interpretation of measures of natural selection. Because of its potential importance for such a wide range of topics, we call for heightened empirical and theoretical attention for this neglected dimension in evolutionary and ecological studies.

Non-random gene flow: an underappreciated force in evolution and ecology

Dispersal is an important life-history trait involved in species persistence, evolution, and diversification, yet is one of the least understood concepts in ecology and evolutionary biology. There is a growing realization that dispersal might not involve the random sample of genotypes as is typically assumed, but instead can be enriched for certain genotypes. Here, we review and compare various sources of such non-random gene flow, and summarize its effects on local adaptation and resource use, metapopulation dynamics, adaptation to climate change, biological invasion, and speciation. Given the possible ubiquity and impacts of non-random gene flow, there is an urgent need for the fields of evolution and ecology to test for non-random gene flow and to more fully incorporate its effects into theory.

Adaptive speciation theory: a conceptual review

Speciation—the origin of new species—is the source of the diversity of life. A theory of speciation is essential to link poorly understood macro-evolutionary processes, such as the origin of biodiversity and adaptive radiation, to well understood micro-evolutionary processes, such as allele frequency change due to natural or sexual selection. An important question is whether, and to what extent, the process of speciation is ‘adaptive’, i.e., driven by natural and/or sexual selection. Here, we discuss two main modelling approaches in adaptive speciation theory. Ecological models of speciation focus on the evolution of ecological differentiation through divergent natural selection. These models can explain the stable coexistence of the resulting daughter species in the face of interspecific competition, but they are often vague about the evolution of reproductive isolation. Most sexual selection models of speciation focus on the diversification of mating strategies through divergent sexual selection. These models can explain the evolution of prezygotic reproductive isolation, but they are typically vague on questions like ecological coexistence. By means of an integrated model, incorporating both ecological interactions and sexual selection, we demonstrate that disruptive selection on both ecological and mating strategies is necessary, but not sufficient, for speciation to occur. To achieve speciation, mating must at least partly reflect ecological characteristics. The interaction of natural and sexual selection is also pivotal in a model where sexual selection facilitates ecological speciation even in the absence of diverging female preferences. In view of these results, it is counterproductive to consider ecological and sexual selection models as contrasting and incompatible views on speciation, one being dominant over the other. Instead, an integrative perspective is needed to achieve a thorough and coherent understanding of adaptive speciation.

Explicit experimental evidence for the role of mate guarding in minimizing loss of paternity in the Seychelles warbler

Extra–pair copulations (EPCs) (copulations outside the pair bond) resulting in extra–pair fertilizations (EPFs) are widespread in birds. To increase reproductive success, males should not only seek EPCs, but also prevent their females from having EPFs. Male Seychelles warblers (Acrocephalus sechellensis) follow their partner closely during the period when these females are most receptive (fertile period). The Seychelles warbler is the first species to offer explicit experimental evidence that mate guarding functions as paternity guarding: in territories where free–living males were induced to stop mate guarding during the pair females fertile period, the rates of intrusions by other males and successful EPCs (male mounting female) were significantly higher than those observed in the control group and in the absence of mate guarding the frequency of successful EPCs increased significantly with local male density. Male warblers do not assure their paternity through frequent copulations to devalue any sperm from other males: males do not copulate with their partners immediately following a successful EPC obtained by their partners, the frequency of successful within–pair copulations does not increase with the frequency of successful EPCs and females initiate all successful copulations and are capable of resisting copulation attempts.

Comparisons between QST and FST—how wrong have we been?

The comparison between quantitative genetic divergence (QST) and neutral genetic divergence (FST) among populations has become the standard test for historical signatures of selection on quantitative traits. However, when the mutation rate of neutral markers is relatively high in comparison with gene flow, estimates of FST will decrease, resulting in upwardly biased comparisons of QST vs. FST. Reviewing empirical studies, the difference between QST and FST is positively related to marker heterozygosity. After refuting alternative explanations for this pattern, we conclude that marker mutation rate indeed has had a biasing effect on published QST–FST comparisons. Hence, it is no longer clear that populations have commonly diverged in response to divergent selection. We present and discuss potential solutions to this bias. Comparing QST with recent indices of neutral divergence that statistically correct for marker heterozygosity (Hedrick’s G′st and Jost’s D) is not advised, because these indices are not theoretically equivalent to QST. One valid solution is to estimate FST from neutral markers with mutation rates comparable to those of the loci underlying quantitative traits (e.g. SNPs). QST can also be compared to ΦST (PhiST) of amova, as long as the genetic distance among allelic variants used to estimate ΦST reflects evolutionary history: in that case, neutral divergence is independent of mutation rate. In contrast to their common usage in comparisons of QST and FST, microsatellites typically have high mutation rates and do not evolve according to a simple evolutionary model, so are best avoided in QST–FST comparisons.

If FST does not measure neutral genetic differentiation, then comparing it with QST is misleading. Or is it?

The comparison between neutral genetic differentiation (FST) and quantitative genetic differentiation (QST) is commonly used to test for signatures of selection in population divergence. However, there is an ongoing discussion about what FST actually measures, even resulting in some alternative metrics to express neutral genetic differentiation. If there is a problem with FST, this could have repercussions for its comparison with QST as well. We show that as the mutation rate of the neutral marker increases, FST decreases: a higher within‐population heterozygosity (He) yields a lower FST value. However, the same is true for QST: a higher mutation rate for the underlying QTL also results in a lower QST estimate. The effect of mutation rate is equivalent in QST and FST. Hence, the comparison between QST and FST remains valid, if one uses neutral markers whose mutation rates are not too high compared to those of quantitative traits. Usage of highly variable neutral markers such as hypervariable microsatellites can lead to serious biases and the incorrect inference that divergent selection has acted on populations. Much of the discussion on FST seems to stem from the misunderstanding that it measures the differentiation of populations, whereas it actually measures the fixation of alleles. In their capacity as measures of population differentiation, Hedrick’s G′ST and Jost’s D reach their maximum value of 1 when populations do not share alleles even when there remains variation within populations, which invalidates them for comparisons with QST.

Why is there variation in baseline glucocorticoid levels

In a recent article in TREE, Bonier and colleagues [1] reviewed the support for the Cort-Fitness Hypothesis, which states that baseline glucocorticoid (cort) levels are elevated in individuals, or populations, that experience challenging conditions, therefore signalling low future fitness. The idea is that the optimal level of resources allocated towards self-maintenance (immediate survival) versus long-term survival and/or reproduction differs across environments, with selection favouring individuals investing in self-maintenance when the environment becomes ‘challenging.’ The hypothesis states that this re-allocation of resources can be achieved by altering baseline levels of cort.

Population differentiation and restricted gene flow in Spanish crossbills: not isolation-by-distance but isolation-by-ecology.

Divergent selection stemming from environmental variation may induce local adaptation and ecological speciation whereas gene flow might have a homogenizing effect. Gene flow among populations using different environments can be reduced by geographical distance (isolation‐by‐distance) or by divergent selection stemming from resource use (isolation‐by‐ecology). We tested for and encountered phenotypic and genetic divergence among Spanish crossbills utilizing different species of co‐occurring pine trees as their food resource. Morphological, vocal and mtDNA divergence were not correlated with geographical distance, but they were correlated with differences in resource use. Resource diversity has now been found to repeatedly predict crossbill diversity. However, when resource use is not 100% differentiated, additional characters (morphological, vocal, genetic) must be used to uncover and validate hidden population structure. In general, this confirms that ecology drives adaptive divergence and limits neutral gene flow as the first steps towards ecological speciation, unprevented by a high potential for gene flow.

A double test of the parasite manipulation hypothesis in a burrowing bivalve

Abstract. The parasite manipulation hypothesis predicts that parasites should be selected to manipulate host behaviour to facilitate transmission to the next host. The bivalve Macoma balthica burrows less deep when parasitized by the trematode Parvatrema affinis. Shallow burrowing increases the likelihood of ingestion by birds, their final hosts, and therefore this has been interpreted as manipulation by the parasite. When unparasitized, M. balthica displays seasonal changes in burrowing depth, becoming less accessible to predators in winter. If shallow burrowing of parasitized individuals is due to direct manipulation by the parasite, the availability of parasitized individuals should be high throughout the year, or at least especially in the season when most birds are present and potential transmission rates are highest. We compared burrowing depths of parasitized and unparasitized individuals in a single population during seven consecutive years. Parasitized individuals showed reduced burrowing depths but, in contrast to the prediction, the effect of parasites on availability to predators was smallest, not largest, in the season with the highest bird numbers. The parasite P. affinis competes for energy with the host, and M. balthica with low energy stores are known to reduce depth of burrowing. When we included size-corrected somatic ash-free dry mass (as an estimate of the energy stores) in our statistical analysis, the effect of infection on burrowing depth disappeared. Thus the effect of infection on burrowing depth is likely to be an unavoidable, indirect effect of the channelling of energy towards the parasite, causing the starving individual to take greater risks in the acquisition of food. Since both the seasonal pattern and the magnitude of increased availability of parasitized individuals are inadequate, the increased exposure of parasitized M. balthica to the final host does not seem to represent an example of adaptive host manipulation by the parasite.