Amber M. Rice

Hybridization and speciation

Hybridization has many and varied impacts on the process of speciation. Hybridization may slow or reverse differentiation by allowing gene flow and recombination. It may accelerate speciation via adaptive introgression or cause near‐instantaneous speciation by allopolyploidization. It may have multiple effects at different stages and in different spatial contexts within a single speciation event. We offer a perspective on the context and evolutionary significance of hybridization during speciation, highlighting issues of current interest and debate. In secondary contact zones, it is uncertain if barriers to gene flow will be strengthened or broken down due to recombination and gene flow. Theory and empirical evidence suggest the latter is more likely, except within and around strongly selected genomic regions. Hybridization may contribute to speciation through the formation of new hybrid taxa, whereas introgression of a few loci may promote adaptive divergence and so facilitate speciation. Gene regulatory networks, epigenetic effects and the evolution of selfish genetic material in the genome suggest that the Dobzhansky–Muller model of hybrid incompatibilities requires a broader interpretation. Finally, although the incidence of reinforcement remains uncertain, this and other interactions in areas of sympatry may have knock‐on effects on speciation both within and outside regions of hybridization.

FIELD AND EXPERIMENTAL EVIDENCE FOR COMPETITION'S ROLE IN PHENOTYPIC DIVERGENCE

Abstract Resource competition has long been viewed as a major cause of phenotypic divergence within and between species. Theory predicts that divergence arises because natural selection favors individuals that are phenotypically dissimilar from their competitors. Yet, there are few conclusive tests of this key prediction. Drawing on data from both natural populations and a controlled experiment, this paper presents such a test in tadpoles of two species of spadefoot toads (Spea bombifrons and S. multiplicata). These two species show exaggerated divergence in trophic morphology where they are found together (mixed-species ponds) but not where each is found alone (pure-species ponds), suggesting that they have undergone ecological character displacement. Moreover, in pure-species ponds, both species exhibit resource polymorphism. Using body size as a proxy for fitness, we found that in pure-species ponds disruptive selection favors extreme trophic phenotypes in both species, suggesting that intraspecific competition for food promotes resource polymorphism. In mixed-species ponds, by contrast, we found that trophic morphology was subject to stabilizing selection in S. multiplicata and directional selection in S. bombifrons. A controlled experiment revealed that the more similar an S. multiplicata was to its S. bombifrons tankmate in resource use, the worse was its performance. These results indicate that S. multiplicata individuals that differ from S. bombifrons would be selectively favored in competition. Our data therefore demonstrate how resource competition between phenotypically similar individuals can drive divergence between them. Moreover, our results indicate that how competition contributes to such divergence may be influenced not only by the degree to which competitors overlap in resource use, but also by the abundance and quality of resources. Finally, our finding that competitively mediated disruptive selection may promote resource polymorphism has potentially important implications for understanding how populations evolve in response to heterospecific competitors. In particular, once a population evolves resource polymorphism, it may be more prone to undergo ecological character displacement.

ECOLOGICAL OPPORTUNITY AND PHENOTYPIC PLASTICITY INTERACT TO PROMOTE CHARACTER DISPLACEMENT AND SPECIES COEXISTENCE

We investigated the roles of resource availability and phenotypic plasticity in promoting ecological character displacement (i.e., trait evolution stemming from resource competition between species). Because ecological character displacement generates new populations that differ in resource use, this process should only occur when exploitable resources are available. We tested this hypothesis in two species of spadefoot toads (Spea bombifrons and S. multiplicata) whose tadpoles use phenotypic plasticity to develop into either an omnivore morph, which specializes on detritus, or a physically distinctive carnivore morph, which specializes on shrimp. Both species grow best on shrimp, but when reared together, S. bombifrons outcompetes S. multiplicata for shrimp and S. multiplicata outcompetes S. bombifrons for detritus. We found that when each species occurred alone in the field, they produced similar proportions of omnivores and carnivores. When the two species occurred together, however, they underwent ecological character displacement in larval development, with S. multiplicata producing mostly omnivores, and S. bombifrons producing mostly carnivores. We combined observations of natural populations with experiments to evaluate whether such character displacement was only possible when both shrimp and detritus were relatively abundant. Mixed-species ponds contained abundant detritus and shrimp, in contrast with nearby pure-species ponds, which were deficient in one resource. Experiments revealed that S. multiplicata competed poorly when detritus was rare and that S. bombifrons competed poorly when shrimp was rare. In nature, when one of these two resources was scarce, one species was missing, perhaps through competitive exclusion by the species that was the superior competitor for the remaining resource. Thus, ecological character displacement and, therefore, coexistence of close competitors, was only possible when diverse resources were available. Finally, even if exploitable resources are available, character displacement is not guaranteed to transpire if species cannot utilize such resources expeditiously. Phenotypic plasticity provides a general and important mechanism for facilitating resource partitioning. Thus, by facilitating shifts in resource use, phenotypic plasticity and ecological opportunity may often interact to promote divergence and coexistence of competitors.

Speciation in Ficedula flycatchers.

Speciation in animals often requires that population divergence goes through three major evolutionary stages, i.e. ecological divergence, development of sexual isolation and the build-up of genetic incompatibility. There is theoretical consensus regarding favourable conditions required for speciation to reach its final and irreversible stage, but empirical tests remain rare. Here, we review recent research on processes of speciation, based on studies in hybrid zones between collared (Ficedula albicollis) and pied flycatchers (Ficedula hypoleuca). A major advantage of this study system is that questions concerning all three major sources of reproductive isolation and their interconnections can be addressed. We conclude that (i) ecological divergence is caused by divergence in life-history traits, (ii) females prefer mates of their own species based on differences in both plumage and song characteristics, (iii) male plumage characteristics have diverged but their song has converged in sympatry, (iv) there is genetic incompatibility in accordance with Haldanes rule, and (v) the Z-chromosome appears to be a hotspot for genes involved in sexual isolation and genetic incompatibility. We discuss how identification of the genes underlying the three major sources of reproductive isolation can be used to draw conclusions about links between the processes driving their evolution.

A guide to the genomics of ecological speciation in natural animal populations

Interest in ecological speciation is growing, as evidence accumulates showing that natural selection can lead to rapid divergence between subpopulations. However, whether and how ecological divergence can lead to the buildup of reproductive isolation remains under debate. What is the relative importance of natural selection vs. neutral processes? How does adaptation generate reproductive isolation? Can ecological speciation occur despite homogenizing gene flow? These questions can be addressed using genomic approaches, and with the rapid development of genomic technology, will become more answerable in studies of wild populations than ever before. In this article, we identify open questions in ecological speciation theory and suggest useful genomic methods for addressing these questions in natural animal populations. We aim to provide a practical guide for ecologists interested in incorporating genomic methods into their research programs. An increased integration between ecological research and genomics has the potential to shed novel light on the origin of species.

Does character displacement initiate speciation? Evidence of reduced gene flow between populations experiencing divergent selection

Character displacement – trait evolution stemming from selection to lessen resource competition or reproductive interactions between species – has long been regarded as important in finalizing speciation. By contrast, its role in initiating speciation has received less attention. Yet because selection for character displacement should act only where species co‐occur, individuals in sympatry will experience a different pattern of selection than conspecifics in allopatry. Such divergent selection might favour reduced gene flow between conspecific populations that have undergone character displacement and those that have not, thereby potentially triggering speciation. Here, we explore these ideas empirically by focusing on spadefoot toads, Spea multiplicata, which have undergone character displacement, and for which character displacement appears to cause post‐mating isolation between populations that are in sympatry with a heterospecific and those that are in allopatry. Using mitochondrial sequence data and nuclear microsatellite genotypes, we specifically asked whether gene flow is reduced between populations in different selective environments relative to that between populations in the same selective environment. We found a slight, but statistically significant, reduction in gene flow between selective environments, suggesting that reproductive isolation, and potentially ecological speciation, might indeed evolve as an indirect consequence of character displacement. Generally, character displacement may play a largely underappreciated role in instigating speciation.

Character displacement: in situ evolution of novel phenotypes or sorting of pre‐existing variation?

Character displacement – the divergence of traits between species in response to competition for resources or mates – has long been viewed as a major cause of adaptive diversification and species coexistence. Yet, we lack answers to basic questions concerning the causes and consequences of character displacement, not the least of which is why some species are more prone than others to undergo character displacement. Here, we address these questions by describing how character displacement can proceed through two nonexclusive routes that differ in the source of phenotypic variation, and, hence, in the ease with which character displacement may unfold. During in situ evolution of novel phenotypes, new traits that are divergent from a heterospecific competitor are generated and spread in sympatry. During sorting of pre‐existing variation, such traits are initially favoured in allopatry before the two species encounter one another. Later, when they come into contact, character displacement transpires when these pre‐existing divergent phenotypes increase in frequency in sympatry relative to allopatry. Because such sorting of pre‐existing variation should unfold relatively rapidly, we suggest that species that express resource or mating polymorphism prior to interactions with heterospecifics may be more prone to undergo character displacement. We discuss the key differences between these two routes, review possible examples of each, and describe how the distinction between them provides unique insights into the evolutionary consequences of species interactions, the origins of diversity, and the factors that govern species coexistence.

POSITIVE FEEDBACK BETWEEN ECOLOGICAL AND REPRODUCTIVE CHARACTER DISPLACEMENT IN A YOUNG AVIAN HYBRID ZONE

Character displacement can reduce costly interspecific interactions between young species. We investigated the mechanisms behind divergence in three key traits—breeding habitat choice, timing of breeding, and plumage coloration—in Ficedula flycatchers. We found that male pied flycatchers became expelled from the preferred deciduous habitat into mixed forest as the superior competitor, collared flycatchers, increased in numbers. The peak in food abundance differs between habitats, and the spatial segregation was paralleled by an increased divergence in timing of breeding between the two species. Male pied flycatchers vary from brown to black with brown coloration being more frequent in sympatry with collared flycatchers, a pattern often proposed to result from selection against hybridization, that is, reinforcement. In contrast to this view, we show that brown male pied flycatchers more often hybridize than black males. Male pied flycatcher plumage coloration influenced the territory obtained in areas of co‐occurrence with collared flycatchers, and brown male pied flycatchers experienced higher relative fitness than black males when faced with heterospecific competition. We suggest that allopatric divergence in resource defense ability causes a feedback loop at secondary contact where male pied flycatchers with the most divergent strategy compared to collared flycatchers are favored by selection.

Estimation of linkage disequilibrium and interspecific gene flow in Ficedula flycatchers by a newly developed 50k single‐nucleotide polymorphism array

With the access to draft genome sequence assemblies and whole‐genome resequencing data from population samples, molecular ecology studies will be able to take truly genome‐wide approaches. This now applies to an avian model system in ecological and evolutionary research: Old World flycatchers of the genus Ficedula, for which we recently obtained a 1.1 Gb collared flycatcher genome assembly and identified 13 million single‐nucleotide polymorphism (SNP)s in population resequencing of this species and its sister species, pied flycatcher. Here, we developed a custom 50K Illumina iSelect flycatcher SNP array with markers covering 30 autosomes and the Z chromosome. Using a number of selection criteria for inclusion in the array, both genotyping success rate and polymorphism information content (mean marker heterozygosity = 0.41) were high. We used the array to assess linkage disequilibrium (LD) and hybridization in flycatchers. Linkage disequilibrium declined quickly to the background level at an average distance of 17 kb, but the extent of LD varied markedly within the genome and was more than 10‐fold higher in ‘genomic islands’ of differentiation than in the rest of the genome. Genetic ancestry analysis identified 33 F1 hybrids but no later‐generation hybrids from sympatric populations of collared flycatchers and pied flycatchers, contradicting earlier reports of backcrosses identified from much fewer number of markers. With an estimated divergence time as recently as <1 Ma, this suggests strong selection against F1 hybrids and unusually rapid evolution of reproductive incompatibility in an avian system.

AN EXPERIMENTAL TEST OF CHARACTER DISPLACEMENT'S ROLE IN PROMOTING POSTMATING ISOLATION BETWEEN CONSPECIFIC POPULATIONS IN CONTRASTING COMPETITIVE ENVIRONMENTS

Abstract Ecological character displacement takes place when two closely related species co-occur in only part of their geographical range, and selection to minimize competition between them promotes divergence in resource-use traits in sympatry but not in allopatry. Because populations sympatric with the heterospecific competitor will experience a different competitive environment than conspecific populations in allopatry, conspecific populations from these two competitive environments will also diverge in resource traits as an indirect consequence of interspecific ecological character displacement. Ultimately, ecologically dependent postmating isolation may arise between conspecific populations from these divergent competitive environments if offspring produced by matings between them are competitively inferior in either type of competitive environment. Yet, there are no direct tests of character displacements role in initiating such postmating isolation. Here, we present a test by comparing the phenotypes and performances of spadefoot toad tadpoles produced from between-competitive-environment (BCE) matings versus those produced from within-competitive-environment (WCE) matings. When raised with naturally occurring competitors, BCE offspring grew significantly less and were significantly smaller than WCE offspring. BCE offspring generally performed worse even when raised alone, suggesting that they may have harbored intrinsic genetic incompatibilities. Moreover, the difference in growth and body size of BCE versus WCE offspring was significantly greater when each was raised with competitors than when each was raised alone, suggesting that BCE tadpoles were competitively inferior to WCE tadpoles. Presumably, this enhanced difference arose because BCE tadpoles produced an intermediate resource-use phenotype that is less well adapted to either competitive environment. Because larval size is under strong, positive, directional selection, reduced growth and size of BCE offspring may diminish gene flow between populations in divergent competitive environments, thereby generating postmating isolation. Thus, postmating isolation between conspecific populations, and possibly even speciation, may arise as a by-product of interactions between species.