The evolution of landscape genetics.

The main objective of this special section is not to review the broad field of landscape genetics, but to provide a glimpse of how the developing landscape genetics perspective has the potential to change the way we study evolution. Evolutionary landscape genetics is the study of how migration and population structure affects evolutionary processes. As a field it dates back to Sewall Wright and the origin of theoretical population genetics, but empirical tests of adaptive processes of evolution in natural landscapes have been rare. Now, with recent developments in technology, methodology, and modeling tools, we are poised to trace adaptive genetic variation across space and through time. Not only will we see more empirical tests of classical theory, we can expect to see new phenomena emerging, as we reveal complex interactions among evolutionary processes as they unfold in natural landscapes.

Comparative landscape genetics and the adaptive radiation of Darwin's finches: the role of peripheral isolation.

We use genetic divergence at 16 microsatellite loci to investigate how geographical features of the Galápagos landscape structure island populations of Darwin's finches. We compare the three most genetically divergent groups of Darwin's finches comprising morphologically and ecologically similar allopatric populations: the cactus finches (Geospiza scandens and Geospiza conirostris), the sharp-beaked ground finches (Geospiza difficilis) and the warbler finches (Certhidea olivacea and Certhidea fusca). Evidence of reduced genetic diversity due to drift was limited to warbler finches on small, peripheral islands. Evidence of low levels of recent interisland migration was widespread throughout all three groups. The hypothesis of distance-limited dispersal received the strongest support in cactus and sharp-beaked ground finches as evidenced by patterns of isolation by distance, while warbler finches showed a weaker relationship. Support for the hypothesis that gene flow constrains morphological divergence was only found in one of eight comparisons within these groups. Among warbler finches, genetic divergence was relatively high while phenotypic divergence was low, implicating stabilizing selection rather than constraint due to gene flow. We conclude that the adaptive radiation of Darwin's finches has occurred in the presence of ongoing but low levels of gene flow caused by distance-dependent interisland dispersal. Gene flow does not constrain phenotypic divergence, but may augment genetic variation and facilitate evolution due to natural selection. Both microsatellites and mtDNA agree in that subsets of peripheral populations of two older groups are genetically more similar to other species that underwent dramatic morphological change. The apparent decoupling of morphological and molecular evolution may be accounted for by a modification of Lack's two-stage model of speciation: relative ecological stasis in allopatry followed by secondary contact, ecological interactions and asymmetric phenotypic divergence.

Hybridization in the recent past.

The question we address in this article is how hybridization in the recent past can be detected in recently evolved species. Such species may not have evolved genetic incompatibilities and may hybridize with little or no fitness loss. Hybridization can be recognized by relatively small genetic differences between sympatric populations because sympatric populations have the opportunity to interbreed whereas allopatric populations do not. Using microsatellite DNA data from Darwin's finches in the Galapagos archipelago, we compare sympatric and allopatric genetic distances in pairs of Geospiza and Camarhynchus species. In agreement with the hybridization hypothesis, we found a statistically strong tendency for a species to be more similar genetically to a sympatric relative than to allopatric populations of that relative. Hybridization has been studied directly on two islands, but it is evidently more widespread in the archipelago. We argue that introgressive hybridization may have been a persistent feature of the adaptive radiation through most of its history, facilitating evolutionary diversification and occasionally affecting both the speed and direction of evolution.

Convergent evolution of Darwin's finches caused by introgressive hybridization and selection.

Between 1973 and 2003 mean morphological features of the cactus finch, Geospiza scandens, and the medium ground finch, G. fortis, populations on the Galápagos island of Daphne Major were subject to fluctuating directional selection. An increase in bluntness or robustness in the beak of G. scandens after 1990 can only partly be explained by selection. We use 16 microsatellite loci to test predictions of the previously proposed hypothesis that introgressive hybridization contributed to the trend, resulting in genes flowing predominantly from G. fortis to G. scandens. To identify F1 hybrids and backcrosses we use pedigrees where known, supplemented by the results of assignment tests based on 14 autosomal loci when parents were not known. We analyze changes in morphology and allelic composition in the two populations over a period of 15-20 years. With samples that included F1 hybrids and backcrosses, the G. scandens population became more similar to the G. fortis population both genetically and morphologically. Gene flow between species was estimated to be three times greater from G. fortis to G. scandens than in the opposite direction, resulting in a 20% reduction in the genetic difference between the species. Nevertheless, removing identified F1 hybrids and backcrosses from the total sample and reanalyzing the traits did not eliminate the convergence. The two species also converged in beak shape by 22.2% and in body size by 45.5%. A combination of introgressive hybridization and selection jointly provide the best explanation of convergence in morphology and genetic constitution under the changed ecological conditions following a major El Niño event in 1983. The study illustrates how species without postmating barriers to gene exchange can alternate between convergence and divergence when environmental conditions oscillate.

Neutral locus heterozygosity, inbreeding, and survival in Darwin's ground finches (Geospiza fortis and G. scandens).

Comprehensive long-term studies of isolated populations provide valuable comparative data that may be used to evaluate different methods for quantifying the relationship between genetic diversity and fitness. Here, we report on data collected from large and well-characterized cohorts of the two numerically dominant species of Darwin's finches on Isla Daphne Major, Galápagos, Ecuador - Geospiza fortis and G. scandens. Multilocus microsatellite (SSR) genetic diversity estimates (heterozygosity and d2) and pedigree-based estimates of the inbreeding coefficient (f) were compared to each other and to two fitness components: lifespan and recruitment. In the larger sample of G. fortis, heterozygosity (H) was correlated with both fitness components, but no relationship was detected in the smaller sample of G. scandens. Analyses of the inbreeding coefficient detected highly significant relationships between f and recruitment, but no relationship between f and overall lifespan. The d2 statistic showed no relationship to either fitness component. When the two SSR-based estimators were compared to f, d2 was correlated with f in G. fortis in the predicted direction, while in G. scandens the relationship was positive. Multilocus heterozygosity was correlated with f in G. fortis but not in the G. scandens sample. A pedigree simulation demonstrated that the variation in true autozygosity can be large among individuals with the same level of inbreeding. This observation may supplement the interpretation of patterns relevant to the local (locus-specific) and general (genome-wide) effects hypotheses, which have been proposed to explain the mechanism responsible for associations between genetic diversity and fitness.

Heritability of morphological traits in Darwin's finches: misidentified paternity and maternal effects.

We studied the influence of extra-pair paternity on heritability estimates of morphological traits in a population of the Medium Ground Finch (Geospiza fortis) on Isla Daphne Major, Galápagos. Data from eight microsatellite loci were used to determine parentage. Six morphological traits measured on each finch were represented by two separate principal components analyses, one for the three bill measurements and one for the body size measurements. Heritabilities were calculated using weighted regressions of offspring on their parents and also offspring on their grandparents. We found that 20% of all offspring were extra-pair young but all offspring matched their mothers. Heritabilities derived from midparent-offspring regressions were all high and significantly different from zero. Removing all extra-pair young from the data set increased father-offspring regressions by an average of 21%, but mother-offspring resemblance still exceeded father-offspring resemblance by up to 42%. These results and grandparent-offspring regressions provide evidence for maternal effects, comparable in magnitude to those reported in other studies of wild birds.

A population founded by a single pair of individuals: establishment, expansion, and evolution.

Events occurring at the founding of a population, and in the next few generations, are potentially of great importance for the future evolution of the population. This study reports demographic, genetic, and morphological changes that took place during and after the colonization of the small Galápagos island of Daphne Major by three male and two female large ground finches, Geospiza magnirostris, at the end of 1982. Using assignment tests with microsatellite DNA data we demonstrate heterogeneity among the immigrants. Their sources included both a near island (Santa Cruz) and a far island (Marchena). However, almost all immigrants that stayed to breed were from an intermediate island (Santiago) and its satellites. Song may have been responsible for this selectivity. Mean heterozygosity stayed roughly constant over the next 15 years while allelic diversity almost doubled, after an initial decline, as the breeding population increased to a maximum of 30 pairs. Although close inbreeding occurred, with a reduction in heterozygosity, an expected net decline in heterozygosity did not occur, for two reasons: it was counteracted by continuing gene flow from immigrants at a low rate, and inbred birds (in one cohort) were at a selective disadvantage. An abrupt step-function shift in beak shape occurred after 9 years. Thus the study provides evidence of drift and selection causing morphological and genetic divergence in the establishment of a new population and in the first few generations.

Habitat structure determines competition intensity and invasion success in gecko lizards.

Species diversity is correlated with structural complexity in many animal communities; however, experimental tests of the mechanisms underlying this important relationship are rare, especially in terrestrial communities. We manipulated physical features of the habitat of gecko lizards and measured the effect on exploitation competition for insects. Increasing both the dispersion of food resources and microhabitat topography dramatically reduced interspecific competition. Adding topographic structure reduced the advantages of the larger, faster, invasive species. Interindividual spacing decreased, but intraspecific agonistic interference increased in the more territorial, resident species. Human structural alterations of the environment facilitate invasion and competitive displacement in this system. Physical microhabitat structure can potentially affect species interactions through a variety of complex mechanisms.

Mechanisms in the Competitive Success of an Invading Sexual Gecko over an Asexual Native.

The competitive displacement by a sexual gecko species of an asexual resident gecko has been documented over a wide geographic area. To test hypotheses concerning the detailed mechanism of this displacement, an experimental system was developed to follow populations of geckos in a duplicated, controlled environment that closely approximates the natural arena for the competitive interaction. Asymmetric competition occurred only in the presence of light, which attracts a dense concentration of insect food sources. The mechanism of competition was partly due to the behavioral dominance of the larger sexual species over the smaller asexual species in areas near the concentrated food. However, this behavior resulted from an avoidance response of subordinate asexuals rather than overt aggression by the sexual species.