Heredity (2008) 100, 443
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NEWS AND COMMENTARY
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Avian mtDNA diversity?
An alternate explanation for low
mtDNA diversity in birds: an age-old
solution?
AJR Hickey
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Heredity (2008) 100, 443; doi:10.1038/hdy.2008.6; published online 13 February 2008
recent article by Berlin et al. (2007)
A (also reviewed by Marais, 2007)
reported that the low mitochon-
drial variability in birds (relative to
mammals) is most easily explained
by Hill–Robertson effects on the W
chromosome. These authors suggest
selection and linkage between the W
chromosome (in heterogametic females)
and mtDNA act to lower avian mtDNA
diversity. This may well be correct;
however, a well-known biological
phenomenon, which appears unique to
birds, was excluded from these ana-
lyses, and may in fact provide a much
simpler and more plausible explanation.
By comparison to mammals, birds
are remarkable in several physiological
parameters such as athletic perfor-
mance, capacity to regenerate neuronal
damage and their high respiratory
efficiencies. However, perhaps more
remarkable are several metabolic avian
features. Birds have metabolic rates that
are 2- to 2.5-fold greater, and estimated
lifetime energy expenditures 15 times
that of mammals of equivalent body
mass. Not only do birds maintain body
temperatures 3 1C hotter than mam-
mals, but many birds have blood glu-
cose levels 2–4 times that of mammals,
which in part defines them as diabetic
(Holmes et al., 2001). This last feature
occurs without the associated patholo-
gical complications seen in mammals
and highlights considerable protection
from oxidative damage.
With few exceptions, birds are also
very long living relative to body mass,
as many birds live three times longer, or
more, than mammals of equivalent
mass, and birds age slower at the
cellular level (Holmes et al., 2001).
Parrots may live over 100 years, and
even the tiny 5 g broad-billed humming-
bird (Selasphorus platycercus) can live for
14 years (Holmes and Austad, 1995),
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while the maximum recorded lifespan
of a 20 g house mouse is only 4 years
(Holmes et al., 2001). Zoo and wild-
tagging data also can mostly eliminate
confounding influences of reduced pre-
dation through flight (Ricklefs, 1998),
and the ‘exception species’, which are
generally domesticated species, still live
relatively long (for example, chickens
20 years, Cortunix quail 6–7 years)
(Holmes and Austad, 1995).
Just how birds achieve such exemp-
lary resistance to age appears to be
largely explained by different mitochon-
drial properties. In mammals, 2–4% of all
consumed oxygen is released as reactive
oxygen species (ROS, for example,
superoxide O2 , hydroxyl radical OH ,
hydrogen peroxide H2O2) from the
electron transport system (ETS) com-
plexes I and III. In health (and more so
with numerous pathologies), mitochon-
dria are generally the largest source of
ROS (Turrens, 2003). Avian mitochondria
produce considerably less ROS than
mammalian mitochondria, with pigeon
liver and heart mitochondria producing
up to 10-fold less H2O2 than rats (this
depends on respiration state, and ROS
predominates from complexes I and III
as O2 , which is converted to H2O2;
Herrero and Barja, 1997; Barja, 2004).
Furthermore, parrots and canaries show
considerable resistance to lipid peroxida-
tion relative to rodents, and isolated
kidney epithelial cells from other long-
lived bird species are much more resi-
lient to pro-oxidant challenge by para-
quat, H2O2 and 95% O2 with markedly
less DNA damage than mouse cells
(Ogburn et al., 1988). The differences
between birds and mammals should
not also be assumed to be adaptive.
ROS release is not necessarily a by-
product of less efficient ETS function,
as ROS provides feedback to cells
and mitochondria (Barja, 2004), which
explains why antioxidants can often
be of detriment (Lane, 2005). These data
do, however, illustrate increased ROS
protection and lower ROS production in
numerous bird species, which results in
less DNA damage (Barja, 2004).
These avian physiological features
were overlooked by Berlin et al. (2007).
This is surprising given that the mito-
chondrial ETS is juxtaposed to mtDNA,
and that ETS-derived ROS makes
the greatest contribution to mtDNA
damage, and hence diversity (Barja,
2004). Admittedly, ROS production
would be a difficult parameter to
measure for many species, although
ROS production correlates more tightly
with longevity than body mass (Barja,
2004). Therefore, correlation of p with
mammalian and avian longevity may
provide greater insight (note that this
assumes the metabolic theory of age-
ing). Potentially, the lower mitochon-
drial ROS output of bird mitochondria
may provide another and potentially
stronger physiological explanation for
the low mtDNA diversity of birds.
Dr AJR Hickey is at the Proteomics and Biomedicine
Research Group, School of Biological Sciences,
University of Auckland, Auckland, New Zealand.
e-mail: a.hickey@auckland.ac.nz
Barja G (2004). Free radicals and ageing. Trends
Neurosci 27: 3602–3607.
Berlin S, Tomaras D, Charlesworth B (2007). Low
mitochondrial variability in birds may indicate
Hill–Robertson effects on the W chromosome.
Heredity 99: 389–396.
Herrero A, Barja G (1997). Sites and mechanisms
responsible for the low rate of free radical
production of heart mitochondria in the long
lived pigeon. Mech Age Dev 98: 95–111.
Holmes DJ, Austad SN (1995). Birds as models for
the comparative biology of ageing: a prospec-
tus. J Gerontol Biol Sci 50A: B59–B66.
Holmes DJ, Flückiger R, Austad SN (2001).
Comparative biology of ageing in birds: an
update. Exp Gerontol 36: 869–883.
Lane N (2005). Power, Sex and Suicide: Mitochondria
and the Meaning of Life. Oxford University
Press: New York, 368 p.
Marais GAB (2007). The Hill–Robertson effects
extend from nucleus to mitochondria. Heredity
99: 357–358.
Ogburn CE, Austad SN, Holmes DJ, Kiklevich JV,
Gollahon K, Rabinovitch PS, Martin GM
(1988). Culture renal epithelial cells from birds
and mice: enhanced resistance of avian cells to
oxidative stress and DNA damage. J Gerontol
Biol Sci 53A: B287–BB229.
Ricklefs RE (1998). Evolutionary theories of age-
ing: confirmation of a fundamental prediction,
with implications for the genetic basis and
evolution of life span. Am Nat 122: 22–44.
Turrens JF (2003). Mitochondrial formation of
reactive oxygen species. J Physiol (Lond) 552:
335–344.