Ecology and genetics of speciation in Ficedula flycatchers

Birds have for long been popular study objects in speciation research. Being easy to observe in the field, they have traditionally been particularly important in studies of behavioural and ecological factors in speciation, whereas the genetic aspects of the process have been studied in other organisms, such as Drosophila. More recently, however, a stronger genetic focus has been placed on speciation research also in birds. Here, we review ecological, behavioural and genetic studies on speciation in the pied flycatcher (Ficedula hypoleuca) and the collared flycatcher (Ficedula albicollis). These well‐studied birds provide among the few proposed examples of the process of reinforcement of premating isolation, and the evidence for reinforcement is strong. They are further characterized by having strong intrinsic postzygotic barriers (female hybrid sterility), yet the two species appear to be very similar ecologically. This is in stark contrast to another well‐studied bird complex, Darwin’s finches, in which the species differ vastly in ecologically important traits but have no developmental problems arising from genetic incompatibilities, and where no evidence for reinforcement is found. In the flycatchers, sex chromosome linkage of genes affecting traits associated with both pre‐ and postzygotic barriers to gene exchange is likely to facilitate reinforcement. We discuss whether such sex‐linkage may be common in birds. The contrast between flycatchers and Darwin’s finches indicate that speciation in birds cannot always be understood mainly as a result of divergent natural selection (‘ecological speciation’), and generalizations from one system may lead us astray. We discuss to what extent insight from research on the flycatchers may point to fruitful avenues for future research on bird speciation and specifically call for a more systematic effort to simultaneously investigate ecology, behaviour and genetics of birds caught in the process of speciation.     

Darwin's Galápagos finches in modern biology

One of the classic examples of adaptive radiation under natural selection is the evolution of 15 closely related species of Darwin''s finches (Passeriformes), whose primary diversity lies in the size and shape of their beaks. Since Charles Darwin and other members of the Beagle expedition collected these birds on the Galápagos Islands in 1835 and introduced them to science, they have been the subjects of intense research. Many biology textbooks use Darwin''s finches to illustrate a variety of topics of evolutionary theory, such as speciation, natural selection and niche partitioning. Today, as this Theme Issue illustrates, Darwin''s finches continue to be a very valuable source of biological discovery. Certain advantages of studying this group allow further breakthroughs in our understanding of changes in recent island biodiversity, mechanisms of speciation and hybridization, evolution of cognitive behaviours, principles of beak/jaw biomechanics as well as the underlying developmental genetic mechanisms in generating morphological diversity. Our objective was to bring together some of the key workers in the field of ecology and evolutionary biology who study Darwin''s finches or whose studies were inspired by research on Darwin''s finches. Insights provided by papers collected in this Theme Issue will be of interest to a wide audience.     

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

Abstract 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.     

Sexually dimorphic neuron addition to an avian song-control region is not accounted for by sex differences in cell death

Only male zebra finches sing, and several brain regions implicated in song behavior exhibit marked sex differences in neuron number. In one region, the high vocal center (HVC), this dimorphism develops because the incorporation of new neurons is greater in males than in females during the first several weeks after hatching. Although estrogen (E₂) exposure stimulates neuron addition in females, it is not known where (E₂) acts, or to what extent sexual differentiation influences the production, specification, or survival of HVC neurons. In the present study we first reassessed sex and (E₂)-induced differences in cell degeneration within the HVC using the TUNEL technique to identify cells undergoing DNA fragmentation indicative of apoptosis. HVC neuron number, as well as the density and number of TUNEL-labeled and pyknotic cells within the HVC were measured in normal 20- and 30-day-old males and females, and in 30-day-old females implanted with E₂ on posthatch day 18. Although HVC neuron number was greater in males than in females, and was masculinized in E₂ females, no group differences were evident in the absolute number of dying cells. These results indicate that sex differences in cell survival within the HVC do not entirely account for sexually dimorphic neuron addition to this region. Rather, sexual differentiation acts on some HVC neurons before they complete their migration and/or early differentiation. Although the migratory route of HVC neurons is not known, a large number of E₂ receptor-containing cells (ER cells) reside just ventromedial to the HVC and adjacent to the proliferative ventricular zone. Next, we investigated whether these ER cells contribute to early-arising sex differences in HVC neuron addition. By combining [³H] thymidine autoradiography with immunocytochemistry for ERs, we first established that ER-expressing cells are not generated during posthatch sexually dimorphic HVC neuron addition, and thus are not young HVC neurons that transiently express ERs during their migration. Furthermore, in 25-day-old birds we found no sex difference in the density of pyknotic cells among this group of ER cells, suggesting that these cells do not promote the differential survival of HVC neuronal precursors migrating through this region. Rather, ER cells or other cell populations may establish sex differences in HVC neuron number by creating dimorphisms in cellular specification. © 1997 John Wiley & Sons, Inc. J Neurobiol 33: 61–71, 1997     

Carotenoid-based ornamentation and status signaling in the house finch

The status signaling hypothesis (SSH) was devised primarilyto explain the adaptive significance of avian ornamental colorationduring the nonbreeding season. It proposes that conspicuousmale plumage serves as an honest signal of social status withina population of birds. However, to date this hypothesis hasbeen well tested and supported for only one type of plumage coloration, melanin-based coloration. Carotenoid-based pigmentationis known to positively reveal male health and condition duringmolt in a variety of species, but it is poorly understood whetherthis ornament type can also function as a status signal duringthe winter. We tested the SSH in male house finches (Carpodacusmexicanus) by manipulating the carotenoid-based plumage brightnessof first-year males and then pairing unfamiliar birds of differingcoloration in a series of dominance trials in captivity. Manipulated plumage color was unrelated to win/loss outcome in these trials.Similarly, the natural pigmentation of males was a poor predictorof winter dominance; as in other studies with this species,we found only a weak tendency for naturally drab males to dominatenaturally bright males. These results suggest that carotenoid-basedcoloration is not a reliable indicator of social status inmale house finches during the nonbreeding season. In fact, carotenoid-based coloration may function only in mate choice in this species,and it may be retained throughout the year either because timeconstraints preclude a second plumage molt or because it aidsin pair formation that begins in late winter.     

A multispecies BCO2 beak color polymorphism in the Darwin’s finch radiation

1. Download : Download high-res image (210KB)
2. Download : Download full-size image

     

Evidence for rapid downward fecundity selection in an ectoparasite (Philornis downsi) with earlier host mortality in Darwin’s finches

Fecundity selection is a critical component of fitness and a major driver of adaptive evolution. Trade‐offs between parasite mortality and host resources are likely to impose a selection pressure on parasite fecundity, but this is little studied in natural systems. The ‘fecundity advantage hypothesis’ predicts female‐biased sexual size dimorphism whereby larger females produce more offspring. Parasitic insects are useful for exploring the interplay between host resource availability and parasite fecundity, because female body size is a reliable proxy for fecundity in insects. Here we explore temporal changes in body size in the myiasis‐causing parasite Philornis downsi (Diptera: Muscidae) on the Galápagos Islands under conditions of earlier in‐nest host mortality. We aim to investigate the effects of decreasing host resources on parasite body size and fecundity. Across a 12‐year period, we observed a mean of c. 17% P. downsi mortality in host nests with 55 ± 6.2% host mortality and a trend of c. 66% higher host mortality throughout the study period. Using specimens from 116 Darwin's finch nests (Passeriformes: Thraupidae) and 114 traps, we found that over time, P. downsi pupae mass decreased by c. 32%, and male (c. 6%) and female adult size (c. 11%) decreased. Notably, females had c. 26% smaller abdomens in later years, and female abdomen size was correlated with number of eggs. Our findings imply natural selection for faster P. downsi pupation and consequently smaller body size and lower parasite fecundity in this newly evolving host–parasite system.     

Under adverse conditions,older small tree finch males (Camarhynchus parvulus) produce more offspring than younger males

Females of many bird species prefer mating with older males, presumably because they provide superior parental care and possibly superior genes. A previous study found that female small tree finches (Camarhynchus parvulus) preferred pairing with old males and had a higher breeding success when paired with old males because their nests were more concealed, higher up in the canopy and therefore less likely to be depredated. However, causes for brood loss have changed over the last decade: predation of small tree finch nests has decreased, whereas brood losses due to parasitism by the invasive parasitic fly Philornis downsi have increased. In the present study, we investigated (a) how the change in predation and parasitism by P. downsi influenced the breeding success of small tree finches, (b) whether there were still differences in breeding success between young and old males, (c) whether P. downsi infestation had a differential effect on nests of young and old males and (d) whether young and old males differed in foraging success. During 2012–2016, we found an overall low influence of predation and a high influence of P. downsi, but neither differed between nests of young and old males. Nests of old males had more fledglings than those of young males. However, the difference in breeding success disappeared when P. downsi numbers were experimentally reduced by injecting an insecticide into nests. This indicates that older males were able to compensate for the detrimental effects of parasitism.