Morphological ghosts of introgression in Darwin’s finch populations

Many species of plants, animals, and microorganisms exchange genes well after the point of evolutionary divergence at which taxonomists recognize them as species. Genomes contain signatures of past gene exchange and, in some cases, they reveal a legacy of lineages that no longer exist. But genomic data are not available for many organisms, and particularly problematic for reconstructing and interpreting evolutionary history are communities that have been depleted by extinctions. For these, morphology may substitute for genes, as exemplified by the history of Darwin’s finches on the Galápagos islands of Floreana and San Cristóbal. Darwin and companions collected seven specimens of a uniquely large form of Geospiza magnirostris in 1835. The populations became extinct in the next few decades, partly due to destruction of Opuntia cactus by introduced goats, whereas Geospiza fortis has persisted to the present. We used measurements of large samples of G. fortis collected for museums in the period 1891 to 1906 to test for unusually large variances and skewed distributions of beak and body size resulting from introgression. We found strong evidence of hybridization on Floreana but not on San Cristóbal. The skew is in the direction of the absent G. magnirostris. We estimate introgression influenced 6% of the frequency distribution that was eroded by selection after G. magnirostris became extinct on these islands. The genetic residuum of an extinct species in an extant one has implications for its future evolution, as well as for a conservation program of reintroductions in extinction-depleted communities.

Triad hybridization via a conduit species

Introgressive hybridization can affect the evolution of populations in several important ways. It may retard or reverse divergence of species, enable the development of novel traits, enhance the potential for future evolution by elevating levels of standing variation, create new species, and alleviate inbreeding depression in small populations. Most of what is known of contemporary hybridization in nature comes from the study of pairs of species, either coexisting in the same habitat or distributed parapatrically and separated by a hybrid zone. More rarely, three species form an interbreeding complex (triad), reported in vertebrates, insects, and plants. Often, one species acts as a genetic link or conduit for the passage of genes (alleles) between two others that rarely, if ever, hybridize. Demographic and genetic consequences are unknown. Here we report results of a long-term study of interbreeding Darwin’s finches on Daphne Major island, Galápagos.Geospiza fortisacted as a conduit for the passage of genes between two others that have never been observed to interbreed on Daphne:Geospiza fuliginosa, a rare immigrant, andGeospiza scandens, a resident. Microsatellite gene flow fromG. fortisintoG. scandensincreased in frequency during 30 y of favorable ecological conditions, resulting in genetic and morphological convergence.G. fortis,G. scandens, and the derived dihybrids and trihybrids experienced approximately equal fitness. Especially relevant to young adaptive radiations, where species differ principally in ecology and behavior, these findings illustrate how new combinations of genes created by hybridization among three species can enhance the potential for evolutionary change.

Temporally varying disruptive selection in the medium ground finch ( Geospiza fortis )

Disruptive natural selection within populations exploiting different resources is considered to be a major driver of adaptive radiation and the production of biodiversity. Fitness functions, which describe the relationships between trait variation and fitness, can help to illuminate how this disruptive selection leads to population differentiation. However, a single fitness function represents only a particular selection regime over a single specified time period (often a single season or a year), and therefore might not capture longer-term dynamics. Here, we build a series of annual fitness functions that quantify the relationships between phenotype and apparent survival. These functions are based on a 9-year mark–recapture dataset of over 600 medium ground finches ( Geospiza fortis ) within a population bimodal for beak size. We then relate changes in the shape of these functions to climate variables. We find that disruptive selection between small and large beak morphotypes, as reported previously for 2 years, is present throughout the study period, but that the intensity of this selection varies in association with the harshness of environment. In particular, we find that disruptive selection was strongest when precipitation was high during the dry season of the previous year. Our results shed light on climatic factors associated with disruptive selection in Darwin's finches, and highlight the role of temporally varying fitness functions in modulating the extent of population differentiation.

Hybridization increases population variation during adaptive radiation

Adaptive radiations are prominent components of the world’s biodiversity. They comprise many species derived from one or a small number of ancestral species in a geologically short time that have diversified into a variety of ecological niches. Several authors have proposed that introgressive hybridization has been important in the generation of new morphologies and even new species, but how that happens throughout evolutionary history is not known. Interspecific gene exchange is expected to have greatest impact on variation if it occurs after species have diverged genetically and phenotypically but before genetic incompatibilities arise. We use a dated phylogeny to infer that populations of Darwin’s finches in the Galápagos became more variable in morphological traits through time, consistent with the hybridization hypothesis, and then declined in variation after reaching a peak. Some species vary substantially more than others. Phylogenetic inferences of hybridization are supported by field observations of contemporary hybridization. Morphological effects of hybridization have been investigated on the small island of Daphne Major by documenting changes in hybridizing populations of Geospiza fortis and Geospiza scandens over a 30-y period. G. scandens showed more evidence of admixture than G. fortis. Beaks of G. scandens became progressively blunter, and while variation in length increased, variation in depth decreased. These changes imply independent effects of introgression on 2, genetically correlated, beak dimensions. Our study shows how introgressive hybridization can alter ecologically important traits, increase morphological variation as a radiation proceeds, and enhance the potential for future evolution in changing environments.

Adult sex ratio influences mate choice in Darwin’s finches

The adult sex ratio (ASR) is an important property of populations. Comparative phylogenetic analyses have shown that unequal sex ratios are associated with the frequency of changing mates, extrapair mating (EPM), mating system and parental care, sex-specific survival, and population dynamics. Comparative demographic analyses are needed to validate the inferences, and to identify the causes and consequences of sex ratio inequalities in changing environments. We tested expected consequences of biased sex ratios in two species of Darwin’s finches in the Galápagos, where annual variation in rainfall, food supply, and survival is pronounced. Environmental perturbations cause sex ratios to become strongly male-biased, and when this happens, females have increased opportunities to choose high-quality males. The choice of a mate is influenced by early experience of parental morphology (sexual imprinting), and since morphological traits are highly heritable, mate choice is expressed as a positive correlation between mates. The expected assortative mating was demonstrated when theGeospiza scandenspopulation was strongly male-biased, and not present in the contemporaryGeospiza fortispopulation with an equal sex ratio. Initial effects of parental imprinting were subsequently overridden by other factors when females changed mates, some repeatedly. Females of both species were more frequently polyandrous in male-biased populations, and fledged more offspring by changing mates. The ASR ratio indirectly affected the frequency of EPM (and hybridization), but this did not lead to social mate choice. The study provides a strong demonstration of how mating patterns change when environmental fluctuations lead to altered sex ratios through differential mortality.

Rapid hybrid speciation in Darwin’s finches

Homoploid hybrid speciation in animals has been inferred frequently from patterns of variation, but few examples have withstood critical scrutiny. Here we report a directly documented example, from its origin to reproductive isolation. An immigrant Darwin’s finch to Daphne Major in the Galápagos archipelago initiated a new genetic lineage by breeding with a resident finch (Geospiza fortis). Genome sequencing of the immigrant identified it as aG. conirostrismale that originated on Española >100 kilometers from Daphne Major. From the second generation onward, the lineage bred endogamously and, despite intense inbreeding, was ecologically successful and showed transgressive segregation of bill morphology. This example shows that reproductive isolation, which typically develops over hundreds of generations, can be established in only three.

Ecological speciation in Darwin’s finches: Parsing the effects of magic traits

Many recent studies of ecological speciation have focused on “magic trait” scenarios, in which divergent selection on viability traits leads inextricably to corresponding divergence in mechanisms, especially mate recognition systems, that facilitate assortative mating. Speciation however may also proceed via other scenarios, such as when populations experience directly selected or random divergence in mate recognition systems. The relative contributions of magic trait versus other scenarios for speciation remain virtually unexplored. The present study aims to test the relative contribution of the magic trait scenario in the divergence of populations of the medium ground finch Geospiza fortis of Santa Cruz Island, Galapagos. First, we assess differences in G. fortis song between a northern population (Borrero Bay) and a southeastern population (El Garrapatero), differences that we propose (along with other within-island geographic song variations) have arisen via scenarios that do not involve a magic trait scenario. Pairwise comparisons of raw and composite (PC) song parameters, as well as discriminant functions analyses, reveal significant patterns of song divergence between sites. Second, we test the ability of territorial males at Borrero Bay to discriminate songs from the two sites. We find that G. fortis males can discriminate within-island song variants, responding more strongly to local than to “foreign” songs, along 3 raw and 1 composite response measures. Third, we compare these findings to prior data sets on song divergence and discrimination in Santa Cruz G. fortis. These comparisons suggest that song divergence and discrimination are shaped less strongly by geographic sources than by morphological (beak-related) sources. We thus argue that interpopulation song divergence and discrimination, fundamental elements of assortative mating in Darwin’s finches, can be fostered in early stages of divergence under magic trait as well as alternative scenarios for speciation, but with more emphasis on the magic trait scenario, at least for this species on this island.