Darren E. Irwin

The role of phenotypic plasticity in driving genetic evolution.

Models of population divergence and speciation are often based on the assumption that differences between populations are due to genetic factors, and that phenotypic change is due to natural selection. It is equally plausible that some of the differences among populations are due to phenotypic plasticity. We use the metaphor of the adaptive landscape to review the role of phenotypic plasticity in driving genetic evolution. Moderate levels of phenotypic plasticity are optimal in permitting population survival in a new environment and in bringing populations into the realm of attraction of an adaptive peak. High levels of plasticity may increase the probability of population persistence but reduce the likelihood of genetic change, because the plastic response itself places the population close to a peak. Moderate levels of plasticity arise whenever multiple traits, some of which are plastic and others not, form a composite trait involved in the adaptive response. For example, altered behaviours may drive selection on morphology and physiology. Because there is likely to be a considerable element of chance in which behaviours become established, behavioural change followed by morphological and physiological evolution may be a potent force in driving evolution in novel directions. We assess the role of phenotypic plasticity in stimulating evolution by considering two examples from birds: (i) the evolution of red and yellow plumage coloration due to carotenoid consumption; and (ii) the evolution of foraging behaviours on islands. Phenotypic plasticity is widespread in nature and may speed up, slow down, or have little effect on evolutionary change. Moderate levels of plasticity may often facilitate genetic evolution but careful analyses of individual cases are needed to ascertain whether plasticity has been essential or merely incidental to population differentiation.

PHYLOGEOGRAPHIC BREAKS WITHOUT GEOGRAPHIC BARRIERS TO GENE FLOW

Abstract The spatial distribution of genetic markers can be useful both in estimating patterns of gene flow and in reconstructing biogeographic history, particularly when gene genealogies can be estimated. Genealogies based on nonrecombining genetic units such as mitochondrial and chloroplast DNA often consist of geographically separated clades that come into contact in narrow regions. Such phylogeographic breaks are usually assumed to be the result of long-term barriers to gene flow. Here I show that deep phylogeographic breaks can form within a continuously distributed species even when there are no barriers to gene flow. The likelihood of observing phylogeographic breaks increases as the average individual dispersal distance and population size decrease. Those molecular markers that are most likely to show evidence of real geographic barriers are also most likely to show phylogeographic breaks that formed without any barrier to gene flow. These results might provide an explanation as to why some species, such as the greenish warblers (Phylloscopus trochiloides), have phylogeographic breaks in mitochondrial or chloroplast DNA that do not coincide with sudden changes in other traits.

Sexual imprinting, learning and speciation

Learned mate preferences may play an important role in speciation. Sexual imprinting is a process whereby mate preferences are affected by learning at a very young age, usually using a parent as the model. We suggest that while the origins of learning appear to lie in the advantages of individual recognition, sexual imprinting results from selection for recognition of conspecifics. This is because efficient early learning about one’s own species is favoured in the presence of heterospecifics. If different species are hybridizing, both sexual imprinting and learning to avoid heterospecifics during adulthood promote assortative mating and hence speciation. As a result of sexual imprinting, speciation may also be completed in allopatry when divergence between populations is sufficient to prevent interbreeding when the populations reunite, even in the absence of genetic evolution of mate preference. The role of behaviour and learning in completing the speciation process is relatively overlooked. In particular the evolution of sexual imprinting as a result of selection against hybridization warrants more study.

Song variation in an avian ring species.

Abstract.— Divergence of mating signals can occur rapidly and be of prime importance in causing reproductive isolation and speciation. A ring species, in which two reproductively isolated taxa are connected by a chain of intergrading populations, provides a rare opportunity to use spatial variation to reconstruct the history of divergence. I use geographic variation in the song of a likely ring species, the greenish warbler (Phylloscopus trochiloides) to reconstruct the microevolutionary steps that occurred during divergence of a trait that is often important in speciation in birds. Populations of a western Siberian (P. t. viridanus) and an eastern Siberian (P. t. plumbeitarsus) form of the greenish warbler meet, but do not interbreed in central Siberia; these forms are connected by a chain of interbreeding populations extending in a ring to the south around the treeless Tibetan Plateau. I show that: (1) song structure differs greatly between the two Siberian forms, which share the same habitat; (2) song structure changes gradually around the ring; (3) singing behavior is relatively simple in the Himalayas, but becomes increasingly complex to the north, both to the west and east of the Tibetan Plateau; and (4) song varies along independent axes of complexity in the western and eastern south‐north clines. By comparing geographic variation in singing behavior and ecological variables, I distinguish among possible causes of song divergence, including selection based on the acoustic environment, stochastic effects of sexual selection, and selection for species recognition. I suggest that parallel south‐to‐north ecological gradients have caused a greater intensity of sexual selection on song in northern populations and that the stochastic effects of sexual selection have led to divergence in song structure.

The use of AFLP to find an informative SNP: genetic differences across a migratory divide in willow warblers

We used the amplified fragment length polymorphism (AFLP) method to obtain genetic markers distinguishing two subspecies of willow warblers Phylloscopus trochilus that have different migratory behaviours but are not differentiated in mitochondrial DNA or at several microsatellite loci. With the inverse‐polymerase chain reaction (PCR) approach we converted a dominant AFLP‐marker to a codominant single nucleotide polymorphism (SNP). Across Scandinavia we typed 621 birds at the SNP locus AFLP‐WW1 and we found a sigmoid change in allele frequencies centred around 62 degrees latitude. North of the latitudinal cline was a west‐east cline. Both clines are narrower than one would expect from dispersal distances in willow warblers, which suggests that these are maintained by selection. The latitudinal cline at the locus AFLP‐WW1 is paralleled by changes in several other traits, all of which might be maintained by a single selective force. The most plausible selection factor that we have identified is selection against hybrids because of inferior migratory behaviour. The selective force maintaining the east–west cline is less obvious. We discuss alternatives to the selection scenario, involving colonization history and asymmetric gene flow.

Ring species as bridges between microevolution and speciation

A demonstration of how small changes can lead to species-level differences is provided by ring species, in which two reproductively isolated forms are connected by a chain of intermediate populations. We review proposed cases of ring species and the insights they provide into speciation. Ring species have been viewed both as illustrations of the history of divergence of two species from their common ancestor and as demonstrations that speciation can occur in spite of gene flow between the diverging forms. Theoretical models predict that speciation with gene flow can occur when there is divergent ecological selection, and geographical differentiation increases the likelihood of speciation. Thus ring species are ideal systems for research into the role of both ecological and geographical differentiation in speciation, but few examples have been studied in detail. The Greenish warbler is a ring species in which two northward expansions around the Tibetan plateau have been accompanied by parallel evolution in morphology, ecology, and song length and complexity. However, songs have diverged in structure, resulting in a lack of recognition where the reproductively isolated forms come into contact in Siberia. Our analysis suggests that these differences could have arisen even with gene flow, and that parallel rather than divergent ecological changes have led to divergence in sexually selected traits and subsequent speciation.

Call divergence is correlated with geographic and genetic distance in greenish warblers (Phylloscopus trochiloides): a strong role for stochasticity in signal evolution?

Divergence in signalling systems might play a central role in speciation. To assess the importance of possible causes of signal divergence, we examine two types of vocalizations within a geographically variable species complex, the greenish warblers (Phylloscopus trochiloides Sundevall). Calls, which are used by both sexes throughout the year, and songs, which are sung primarily by breeding males, differ distinctly between two distinct Siberian forms. Through a ring of southern populations that connect the northern forms, signal divergence is correlated with both geographic distance and genetic divergence. Calls and songs differ in their particular patterns of geographic variation, probably because of the larger influence of sexual selection on songs than on calls. These patterns are supportive of neither acoustic adaptation nor morphology being major drivers of divergence in vocalizations. Rather, these results support the importance of stochastic evolution of communication systems in the evolution of new species.

Conflicting patterns of mitochondrial and nuclear DNA diversity in Phylloscopus warblers

Molecular variation is often used to infer the demographic history of species, but sometimes the complexity of species history can make such inference difficult. The willow warbler, Phylloscopus trochilus, shows substantially less geographical variation than the chiffchaff, Phylloscopus collybita, both in morphology and in mitochondrial DNA (mtDNA) divergence. We therefore predicted that the willow warbler should harbour less nuclear DNA diversity than the chiffchaff. We analysed sequence data obtained from multiple samples of willow warblers and chiffchaffs for the mtDNA cytochrome b gene and four nuclear genes. We confirmed that the mtDNA diversity among willow warblers is low (π = 0.0021). Sequence data from three nuclear genes (CHD‐Z, AFLP‐WW1 and MC1R) not linked to the mitochondria demonstrated unexpectedly high nucleotide diversity (π values of 0.0172, 0.0141 and 0.0038) in the willow warbler, on average higher than the nucleotide diversity for the chiffchaff (π values of 0.0025, 0.0017 and 0.0139). In willow warblers, Tajimas D analyses showed that the mtDNA diversity, but not the nuclear DNA diversity, has been reduced relative to the neutral expectation of molecular evolution, suggesting the action of a selective sweep affecting the maternally inherited genes. The large nuclear diversity seen within willow warblers is not compatible with processes of neutral evolution occurring in a population with a constant population size, unless the long‐term effective population size has been very large (Ne > 106). We suggest that the contrasting patterns of genetic diversity in the willow warbler may reflect a more complex evolutionary history, possibly including historical demographic fluctuations or historical male‐biased introgression of nuclear genes from a differentiated population of Phylloscopus warblers.

Dramatic intraspecific differences in migratory routes, stopover sites and wintering areas, revealed using light-level geolocators

Migratory divides are contact zones between breeding populations that use divergent migratory routes and have been described in a variety of species. These divides are of major importance to evolution, ecology and conservation but have been identified using limited band recovery data and/or indirect methods. Data from band recoveries and mitochondrial haplotypes suggested that inland and coastal Swainsons thrushes (Catharus ustulatus) form a migratory divide in western North America. We attached light-level geolocators to birds at the edges of this contact zone to provide, to our knowledge, the first direct test of a putative divide using data from individual birds over the entire annual cycle. Coastal thrushes migrated along the west coast to Mexico, Guatemala and Honduras. Some of these birds used multiple wintering sites. Inland thrushes migrated across the Rocky Mountains, through central North America to Columbia and Venezuela. These birds migrated longer distances than coastal birds and performed a loop migration, navigating over the Gulf of Mexico in autumn and around this barrier in spring. These findings support the suggestion that divergent migratory behaviour could contribute to reproductive isolation between migrants, advance our understanding of their non-breeding ecology, and are integral to development of detailed conservation strategies for this group.

Cryptic speciation in a Holarctic passerine revealed by genetic and bioacoustic analyses

There has been much controversy regarding the timing of speciation events in birds, and regarding the relative roles of natural and sexual selection in promoting speciation. Here, we investigate these issues using winter wrens (Troglodytes troglodytes), an unusual example of a passerine with a Holarctic distribution. Geographical variation has led to speculation that the western North American form Troglodytes troglodytes pacificus might be a distinct biological species compared to those in eastern North America (e.g. Troglodytes troglodytes hiemalis) and Eurasia. We located the first known area in which both forms can be found, often inhabiting neighbouring territories. Each male wren in this area sings either western or eastern song, and the differences in song are as distinct in the contact zone as they are in allopatry. The two singing types differ distinctly in mitochondrial DNA sequences and amplified fragment length polymorpism profiles. These results indicate that the two forms are reproductively isolated to a high degree where they co‐occur and are therefore separate species. DNA variation suggests that the initial split between the two species occurred before the Pleistocene, quite long ago for sister species in the boreal forest. Surprisingly, the two forms are similar in morphometric traits and habitat characteristics of territories. These findings suggest that sexual selection played a larger role than habitat divergence in generating reproductive isolation, and raise the possibility that there are other such morphologically cryptic species pairs in North America.