Metabolic ‘engines’ of flight drive genome size reduction in birds

Wright, Natalie A.; Gregory, T. Ryan; Witt, Christopher C.

doi:10.1098/rspb.2013.2780

Cited by 113 publications

(124 citation statements)

References 51 publications

Supporting

Mentioning

110

Contrasting

Order By: Relevance

“…Genome size variation between bird species has been linked to variation in metabolic cost of powered flight, with hummingbirds exhibiting the highest metabolism and smallest genomes (12,100,101), whereas flightless ratite birds display the largest genomes (2,51,102). Our results lend further support to this connection between metabolic rate and genome size reduction.…”

Section: Dna Gain and Loss Analysis Reveals The Elasticity Of Avian Asupporting

confidence: 74%

“…Additionally, the fixation probability of slightly deleterious deletions or insertions would be higher in species with smaller effective population sizes, where natural selection acts less efficiently (3,8). On the other hand, a number of correlative associations between genome size and phenotypic traits, such as cell size (9,10) and metabolic rate associated with powered flight (11,12), suggest that natural selection and adaptive processes also shape genome size evolution. Teasing apart the relative importance of these two forces (drift and selection) requires a better understanding of the mode and processes by which DNA is gained and lost over long evolutionary periods in different taxa.…”

mentioning

confidence: 99%

See 1 more Smart Citation

Dynamics of genome size evolution in birds and mammals

Kapusta

Suh

Feschotte

2017

Proc. Natl. Acad. Sci. U.S.A.

370

358

View full text Add to dashboard Cite

Genome size in mammals and birds shows remarkably little interspecific variation compared with other taxa. However, genome sequencing has revealed that many mammal and bird lineages have experienced differential rates of transposable element (TE) accumulation, which would be predicted to cause substantial variation in genome size between species. Thus, we hypothesize that there has been covariation between the amount of DNA gained by transposition and lost by deletion during mammal and avian evolution, resulting in genome size equilibrium. To test this model, we develop computational methods to quantify the amount of DNA gained by TE expansion and lost by deletion over the last 100 My in the lineages of 10 species of eutherian mammals and 24 species of birds. The results reveal extensive variation in the amount of DNA gained via lineage-specific transposition, but that DNA loss counteracted this expansion to various extents across lineages. Our analysis of the rate and size spectrum of deletion events implies that DNA removal in both mammals and birds has proceeded mostly through large segmental deletions (>10 kb). These findings support a unified "accordion" model of genome size evolution in eukaryotes whereby DNA loss counteracting TE expansion is a major determinant of genome size. Furthermore, we propose that extensive DNA loss, and not necessarily a dearth of TE activity, has been the primary force maintaining the greater genomic compaction of flying birds and bats relative to their flightless relatives.genome size evolution | DNA loss | transposable elements | amniotes | flight T he nature and relative importance of the molecular mechanisms and evolutionary forces underlying genome size variation has been the subject of intense research and debate (1-7). Variation in genome sizes may not always occur at a level where natural selection is strong enough to prevent genetic drift to determine their fate (neutral or effectively neutral variation) (3). Additionally, the fixation probability of slightly deleterious deletions or insertions would be higher in species with smaller effective population sizes, where natural selection acts less efficiently (3,8). On the other hand, a number of correlative associations between genome size and phenotypic traits, such as cell size (9, 10) and metabolic rate associated with powered flight (11, 12), suggest that natural selection and adaptive processes also shape genome size evolution. Teasing apart the relative importance of these two forces (drift and selection) requires a better understanding of the mode and processes by which DNA is gained and lost over long evolutionary periods in different taxa. Thus, establishing an integrated view of the contribution of gain and loss of DNA to genome size variation (or lack thereof) remains an important goal in genome biology (e.g., refs. 1, 2, 13, and 14).Most studies of genome size evolution have focused on taxa with extensive variation in genome sizes, such as flowering plants (15)(16)(17)(18)(19)(20), conifers (21), insects (22-...

show abstract

Section: Dna Gain and Loss Analysis Reveals The Elasticity Of Avian Asupporting

confidence: 74%

mentioning

confidence: 99%

Dynamics of genome size evolution in birds and mammals

Kapusta

Suh

Feschotte

2017

Proc. Natl. Acad. Sci. U.S.A.

370

358

View full text Add to dashboard Cite

show abstract

“…To test the hypothesis that island species had evolved smaller flight muscles than their continental relatives, we weighed the two main flight muscles, the pectoralis major and the supracoracoideus, from more than 8,000 bird carcasses, representing 868 landbird species, 38 of which are restricted to islands (23,24). With all taxa combined, island-restricted species had smaller flight muscles, relative to body Significance Predictable evolutionary trends illuminate mechanisms that affect the diversity of traits and species on the tree of life.…”

Section: Resultsmentioning

confidence: 99%

“…For the comparison of continents versus islands, we used bird specimens that were collected by us and many colleagues using standard museum methods (23,24). Each bird was weighed, and the pectoralis major and supracoracoideus muscles were extracted and weighed.…”

Section: Methodsmentioning

confidence: 99%

Predictable evolution toward flightlessness in volant island birds

Wright

Steadman

Witt

2016

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

139

137

View full text Add to dashboard Cite

Birds are prolific colonists of islands, where they readily evolve distinct forms. Identifying predictable, directional patterns of evolutionary change in island birds, however, has proved challenging. The "island rule" predicts that island species evolve toward intermediate sizes, but its general applicability to birds is questionable. However, convergent evolution has clearly occurred in the island bird lineages that have undergone transitions to secondary flightlessness, a process involving drastic reduction of the flight muscles and enlargement of the hindlimbs. Here, we investigated whether volant island bird populations tend to change shape in a way that converges subtly on the flightless form. We found that island bird species have evolved smaller flight muscles than their continental relatives. Furthermore, in 366 populations of Caribbean and Pacific birds, smaller flight muscles and longer legs evolved in response to increasing insularity and, strikingly, the scarcity of avian and mammalian predators. On smaller islands with fewer predators, birds exhibited shifts in investment from forelimbs to hindlimbs that were qualitatively similar to anatomical rearrangements observed in flightless birds. These findings suggest that island bird populations tend to evolve on a trajectory toward flightlessness, even if most remain volant. This pattern was consistent across nine families and four orders that vary in lifestyle, foraging behavior, flight style, and body size. These predictable shifts in avian morphology may reduce the physical capacity for escape via flight and diminish the potential for small-island taxa to diversify via dispersal.B irds on islands helped to inspire the theory of evolution by natural selection (1, 2), and they continue to illuminate its mechanisms (e.g., ref.3). Some studies have reported that the bodies and bills of island birds systematically shift in size, reflecting evolution toward a generalist niche in species-poor communities (4-8). The tendency for island taxa to converge toward intermediate body size after colonizing islands is known as the island rule (4), but this ecogeographic rule has proven to be an inconsistent predictor of evolutionary trends in island bird populations (9-12). Detailed studies of island radiations have revealed idiosyncratic patterns of body size and bill size evolution among species, with morphological changes attributable to taxon-specific changes in foraging ecology (e.g., ref. 12). This inconsistency raises the question as to whether there are predictable evolutionary trends that apply generally to island birds.The most striking evolutionary trend among island birds is the loss of flight. Transitions to flightlessness are rapid and irreversible (13,14), with each instance involving the substantial reallocation of mass from the forelimbs to the hindlimbs and near elimination of costly flight muscles (15-18). More than 1,000 independent lineages of island birds have lost flight, including rails, parrots, pigeons, owls, waterfowl, and passerines (13-1...

show abstract

“…the sum of the pectoralis major and minor) by the body mass (Wright et al, 2014). Heart and lung indices were calculated by dividing the heart mass and lung mass by the body mass, respectively (Vinogradov and Anatskaya, 2006;Wright et al, 2014).…”

Section: Load-lifting Assaymentioning

confidence: 99%

Flying high: Limits to flight performance by sparrows on the Qinghai-Tibet Plateau

Sun

Ren

et al. 2016

Journal of Experimental Biology

View full text Add to dashboard Cite

Limits to flight performance at high altitude potentially reflect variable constraints deriving from the simultaneous challenges of hypobaric, hypodense and cold air. Differences in flight-related morphology and maximum lifting capacity have been well characterized for different hummingbird species across elevational gradients, but relevant within-species variation has not yet been identified in any bird species. Here we evaluate load-lifting capacity for Eurasian tree sparrow (Passer montanus) populations at three different elevations in China, and correlate maximum lifted loads with relevant anatomical features including wing shape, wing size, and heart and lung masses. Sparrows were heavier and possessed more rounded and longer wings at higher elevations; relative heart and lung masses were also greater with altitude, although relative flight muscle mass remained constant. By contrast, maximum lifting capacity relative to body weight declined over the same elevational range, while the effective wing loading in flight (i.e. the ratio of body weight and maximum lifted weight to total wing area) remained constant, suggesting aerodynamic constraints on performance in parallel with enhanced heart and lung masses to offset hypoxic challenge. Mechanical limits to take-off performance may thus be exacerbated at higher elevations, which may in turn result in behavioral differences in escape responses among populations.

show abstract

Metabolic ‘engines’ of flight drive genome size reduction in birds

Cited by 113 publications

References 51 publications

Dynamics of genome size evolution in birds and mammals

Dynamics of genome size evolution in birds and mammals

Predictable evolution toward flightlessness in volant island birds

Flying high: Limits to flight performance by sparrows on the Qinghai-Tibet Plateau

Contact Info

Product

Resources

About