Download The Heritability of External Morphology in Darwin`s Ground Finches

The Heritability of External Morphology in Darwin's Ground Finches (Geospiza) on Isla
Daphne Major, Galapagos
Author(s): Peter T. Boag
Source: Evolution, Vol. 37, No. 5 (Sep., 1983), pp. 877-894
Published by: Society for the Study of Evolution
Stable URL: http://www.jstor.org/stable/2408404
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Evolution
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EVOLUTION
INTERNATIONAL JOURNAL OF ORGANIC EVOLUTION
PUBLISHED BY
THE SOCIETY FOR THE STUDY OF EVOLUTION
Vol.
37
September,
1983
No.
5
Evolution, 37(5), 1983, pp 877-894
THE HERITABILITY OF EXTERNAL MORPHOLOGY IN DARWIN'S
GROUND FINCHES (GEOSPIZA) ON ISLA
DAPHNE MAJOR, GALAPAGOS
PETER T. BOAG1
Department of Biology, Trent University, Peterborough, Ontario K9J 7B8, Canada
Received October 23, 1981. Revised December 20, 1982
bill length in mm) in terms of a genotypic
value and an environmental deviation, i.e.,
P = G + E, or for the phenotypic variance of a population, Vp = VG + VE. The
genotypic value of an individual can in
turn be partitioned into a breeding value,
a dominance deviation, and an interaction
deviation, i.e., G = A + D + I, or VG =
Ecologists use avian morphological
measurements to develop and test evolu-
tionary theories. The theories are usually
based on genetic models, although little is
known about the inheritance of such char-
acters. In field studies it is commonly assumed that phenotypic variation closely
reflects underlying genetic variation (Grant
VA + VD + VI. Genetic resemblance be-
et al., 1976), while theoreticians some-
et al., 1976; Abbott et al., 1977; Boag and
tween relatives is a function of breeding
values; thus the variance of breeding values (the additive genetic variance or VA
above), is an important property of a pop-
Grant, 1981; Grant, 198 lb) have been
ulation.
times assume that heritabilities are equal
to one (Long, 1974).
P. R. Grant and his colleagues (Grant
studying Darwin's ground finches (Geospiza) in the Galapagos, focusing on relationships between finch morphology and
food supplies. Unlike Mendelian characters such as plumage polymorphisms (Mi-
neau and Cooke, 1979), finch morphology
involves metric characters and is studied
using quantitative genetics (Falconer,
1981). Quantitative genetics describes the
phenotypic value of an individual (e.g., its
1 Present address: Department of Biology,
University, Kingston, Ontario, Canada K7L 3N6.
Heritability in the narrow sense (h2) is
the proportion of the phenotypic variance
which is additive genetic (Falconer, 1981).
The response of a trait to direct selection
is a product of its heritability and the selection differential, i.e., R = h2S (Falconer, 1981). To argue that a metric trait is
capable of evolutionary adaptation to a
changing environment, one must demonstrate the existence of both additive genetic variation and appropriate selection
pressures. Biochemical studies suggest that
a large reservoir of genetic variation exists
in most populations (Nevo, 1978; Clarke,
Queen's
1979; Powell and Taylor, 1979). Attempts
877
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878
PETER
T.
BOAG
have been made to correlate electropho-
responses in other characters (Falconer,
retic or karyotypic variation with mor-
1981). In field studies, natural selection by
phological variation (Soule et al., 1973;
Patton et al., 1975; Rising and Shields,
definition acts on the entire phenotype, and
this complicates analyses of heritability and
1980), but the relationship remains ten-
the response to selection (Lande, 1979). As
tative (Kolata, 1974; Carson, 1976). Like-
an indirect solution to this problem, linear
wise, examples of selection are widespread
combinations of characters based on prin-
(O'Donald, 1973; Berry, 1977 p. 130-131;
cipal components (PCs) have been used
Dhondt et al., 1979; Boag and Grant, 1981;
with Darwin's finches (Boag and Grant,
Grant and Price, 198 1; Johnston and
1981), and thus it is important to dem-
Fleischer, 1981), but there are few verte-
onstrate that such combinations of char-
brate traits of generally accepted ecologi-
acters are themselves heritable. Multi-
cal importance, with both a known quan-
variate approaches to evolutionary
titative genetic basis and a known selection
problems sometimes assume a close correspondence between phenotypic (rp) and
regime.
Why have quantitative genetics not been
genetic (rG) correlations; this is not always
more widely used with natural popula-
justified (Atchley and Rutledge, 1980), although rp and rG matrices may be similar
tions of vertebrates? Certainly long term
studies of individually marked animals
have only recently become available, but
in certain suites of characters (Leamy,
also, quantitative genetics evolved as an
et al., 1981). Such similarity simplifies the
applied science, with control over matings
and the environment individuals develop
evolutionary interpretation of phenotypic
in. The lack of experimental control com-
is useful to partition phenotypic correla-
plicates application of the methodology to
tions into their genetic and environmental
field studies, and the interpretation of field
(rE) components (Falconer, 1981).
1977; Lande, 1979; Arnold, 1981; Atchley
correlations, and hence when possible, it
data. For instance, quantitative genetics
Boag and Grant (1978) found high her-
assumes that environmental deviations are
itabilities for morphological traits in the
independent, random normal deviates. If
medium ground finch (Geospiza fortis)
they depend on the breeding value of an
during 1976 on Isla Daphne Major, Ga-
individual, or if deviations among groups
lapagos. Here I describe the growth and
repeatabilities of the seven traits involved,
re-examine evidence for assortative mat-
of individuals or traits are structured, this
assumption is violated. There has been
concern about such effects in human stud-
ing, and extend the preliminary heritabil-
ies, particularly with respect to genotype-
ity results using additional data from 1978.
environment correlations (Feldman and
I also examine covariation among the
Lewontin, 1975). However, recent avian
characters by calculating rp, rG, and rE
matrices. These analyses confirm that PC 1
field studies (Perrins and Jones, 1974; Boag
and Grant, 1978; Greenwood et al., 1979;
Ojanen et al., 1979; Smith and Zach, 1979;
van Noordwijk et al., 1980; Garnett, 1981)
have produced high heritabilities, with little evidence for genotype-environment
correlations (Smith and Dhondt, 1981;
Dhondt, 1982; Lessells, 1982).
Another problem is that external mor-
is a highly heritable index of overall body
size, which responded to strong selection
on Daphne in 1977 (Boag and Grant,
1981). In addition I provide preliminary
estimates of heritabilities in a second
species of Darwin's finch, the cactus finch
(G. scandens).
phological measurements are usually cor-
METHODS
related. In a laboratory setting one can
Most of the adult G. fortis and G. scandens have been measured and individually
banded on Isla Daphne Major, Galapagos. In 1976 (N = 481) and 1978 (N = 384)
estimate the heritability of a single character, subject it to direct artificial selection, and observe the pattern of correlated
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FINCH
nestlings were banded, and some later
mist-netted and measured. By identifying
marked parents at the nest, one can relate
their measurements to those of their subsequently caught young. Additional details of the field work are described in Boag
(1981).
Seven morphological variables were ex-
amined: weight in grams (WGT), and flattened wing chord (WNG), tarsus length
from the nuchal notch to the lowest undivided scute (TRS), bill length from the
HERITABILITIES
879
involved. Geospiza fortis and scandens
reach asymptotic weight, wing length, and
tarsus length by six weeks of age, while
bill length, depth and width asymptote in
G. fortis by eight weeks after hatching.
Geospiza scandens bills grow more slowly,
with bill length taking up to 12 weeks to
asymptote (Boag, 1981). Geospiza fortis
under eight weeks old were excluded from
the analysis, and as a compromise between sample size and age, the scandens
bill depth at the anterior edge of the nares
analyses excluded young under nine weeks
old. This group had heritabilities similar
to separately analyzed eight and 12 week
in a plane perpendicular to the commis-
old scandens.
sure (BDT), bill width at the widest ex-
To minimize nonrandom associations
between phenotypes and environments,
Smith and Dhondt (1980), Ricklefs and
Peters (1980), and Dhondt (1982) swapped
clutches among parents. This has not yet
been feasible on Daphne, but a less pow-
interior edge of the nares to the tip (BLG),
panse of the lower mandible (BWD), and
bill length at a depth of 4 mm (LA4), measured by marking the upper bill at a total
bill depth of 4 mm, and then measuring
the distance from that plane to the tip, all
measured in mm (Abbott et al., 1977;
Boag, 198 1). LA4 is usually larger in
smaller individuals. After a repeatability
analysis, measurements were averaged for
birds measured on more than one occa-
sion. Corrections were applied to measurements made by P. R. Grant in 1975,
based on adult birds measured by both of
us. A reference group of 10 museum specimens was also used to maintain measurement uniformity during the study.
Repeatabilities were estimated using
variance components from analyses of
variance (ANOVAs) (Sokal and Rohlf,
1969; Falconer, 1981). I used repeatabilities to assess measurement error by catch-
ing 10 G. fortis at Academy Bay, Isla Santa Cruz, and measuring each bird four
times in four hours, in random order and
under typical field conditions. I predicted
upper limits for heritability estimates (Falconer, 1981) by calculating repeatabilities
of adult Daphne finches remeasured during the study. Such long term repeatabilities contain variation due to changes in
measurement technique with time, as well
as growth and abrasion of morphology.
Calculation of heritabilities assumes that
a character is the same structure, in the
same ontogenetic stage, in all individuals
erful, a posteriori check for obvious genotype-environment correlations is to test
for consistent associations between the
morphology of parents and their offspring
under different developmental environments, such as different nesting habitats
or clutch sizes. I tested each character in
males, females, and offspring separately
in four one-way ANOVAs: variation
among three habitats (outer slope, inner
slope, and plateau; see Boag [1981] for
study areas), among dates of first egg laid
(early, middle or late), among clutch sizes,
and among numbers of young fledged. The
84 tests were carried out only on G. fortis
because scandens numbers were too small
when split into the required categories.
Young Darwin's finches cannot be sexed
without performing laparotomies, and thus
all young were pooled, increasing the error
of h2 estimates because of the variation in
broods due to sexual dimorphism (the traits
are 4-8% larger in males compared to females). Smith and Zach (1979) standardized for sex and year in their analysis of
song sparrow (Melospiza melodia) morphology and Greenwood et al. (1979) standardized for annual variation in the heritability of great tit (Parus major) dispersal.
One can also add or multiply by correction
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880
PETER
T.
BOAG
factors (Perrins and Jones, 1974). Stan-
group correlation matrix, which is empha-
dardization may alter regression slopes, so
sized in the Results. Despite strong selec-
where possible a better procedure is to pool
tion in 1977 (Boag and Grant, 198 1), fortis
sums of squares and crossproducts from
covariance matrices for the two years were
the groups of data and calculate pooled
homogeneous (Box's M-test, N = 275,
regressions. I pooled the 1976 and 1978 G.
P > .05).
fortis data, but also discuss the results for
rG and rE matrices were calculated using
each year. These provide a replicated test
standard procedures (Falconer, 198 1), with
for heritabilities based on different parents
the emphasis on the midparent-offspring
and offspring, following a major pertur-
data. In regression-based genetic correla-
bation in 1977 (Boag and Grant, 1981).
tions, there are two cross-covariances pos-
Four methods were used to calculate
sible for each pair of characters, and I used
heritabilities: separate regressions of off-
their arithmetic mean (Van Vleck and
spring on male and female only and mid-
Henderson, 1961):
parent and full sib intraclass correlations
(Becker, 1975; Falconer, 1981). The slope
of the regression of mean offspring mea-
rG = (COVxyl + COVYx1)/
2 V(COVXXCOVY,).
surements on the mean of their parents'
measurements (the midparent value) di-
Here COVx,,, is the covariance between
rectly estimates heritability. The regressions of offspring means on their mother's
ter y' in the offspring. Family size weighting was not used. I followed Cheverud
or father's measurements alone estimate
(1982) in calculating standard errors for rG
single parent heritabilities when multi-
and rE, although his Eq. 4 is somewhat
misleading, and I thus referred also to
plied by two. All regressions used a family
character x in the midparent and charac-
size weighting technique (Falconer, 1963).
ANOVA was used to estimate variance
Reeve (1955).
components for intraclass correlations (So-
from rp matrices using SPSS (Nie et al.,
Principal components were extracted
kal and Rohlf, 1969); full sib heritabilities
1975). PCs summarize linear trends in a
are twice the intraclass correlation, and in
addition to additive genetic variance, contain variance due to nonadditive genetic
and common environment effects.
Only four pairs of G. scandens young
and their parents were measured in 1976.
In 1977 no fortis bred and no scandens
correlated data set, and component scores
typic qualities are most strongly inherited
young survived to be measured (Boag,
multivariate structure with that seen in the
1981). The 1978 scandens were initially
phenotypic correlations.
analyzed in the same fashion as 1978 fortis; because scandens were not subject to
the strong directional selection experi-
calculated for parents and offspring can
be used to suggest which overall pheno(Cheverud, 1981). SPSS was also used to
extract PCs fromfortis rG and rE matrices
(Atchley et al., 1981), to compare their
Log10 scales were used in the correlation
analyses because allometry produces curvilinear relationships between many of
enced byfortis in 1977 (Boag and Grant,
these variables (see also Ricklefs and
1981), I added the four 1976 pairs to the
Travis, 1979). Other analyses showed that
data, and found that heritabilities re-
log10 transformation had little effect on
mained the same.
heritabilities, phenotypic or genetic cor-
Phenotypic correlations of the seven log10
relations, or PC analyses (Kempthorne,
transformed variables were generated using all adults and offspring involved in the
formed covariance matrices were also sim-
1960 p. 12-23). PC analyses of logl0-trans-
univariate heritability calculations, with
ilar to correlation based analyses. Given
separate matrices for the two years of G.
fortis data. The 1976 and 1978fortis data
that many of the quantities involved are
dimensionless and that no character had
were also used to produce a pooled within
a coefficient of variation (CV) over 11%
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FINCH
HERITABILITIES
881
(Table 4), the robustness of these calcu-
TABLE 1. Repeatabilities of Geospiza measure-
lations to differences of scale is not sur-
ments. The Santa Cruz birds are 10 G. fortis each
prising (Lande, 1979).
RESULTS
measured four times on Isla Santa Cruz. The other
data are forfinches captured between 1975 and 1978
on Isla Daphne Major and measured two to four times
Repeatability of Measurements
each. The All group contains males, females and birds
Mechanical measurement error is negligible in the seven characters, as repeat-
P. R. Grant in 1975. N is the number of different
abilities within a single day are high (Ta-
of measurements made.
of uncertain sex, with some measurements made by
individuals measured, followed by the total number
ble 1). Over longer time intervals, weight
changes and seasonal feather and beak
growth or abrasion do alter repeatabili-
ties. Table 1 shows that weight, wing, and
LA4 have lower long term repeatabilities
than tarsus and bill length, depth and
width. G. scandens repeatabilities tend to
be lower than in G. fortis, and females of
both species have lower weight repeatabilities than males.
Phenotypes and Environments
Seven of the 84 ANOVAs across environmental categories were significant in
1976, although there were no strong de-
viations of parent and offspring means in
the same direction in a given environment
(Boag and Grant, 1978). In 1978, males
living on the inner slopes were largest, significantly so for tarsus length (Duncan
Multiple Range tests, P < .05). Females
showed a similar, but not significant pattern. Inner slope young were significantly
larger than other young except for bill
length and width. Inner slope young were
also older, but when age was controlled
for as a covariate, the area effect remained
significant.
There were no significant differences in
1978 among early, middle, or late season
nesters. 1978 males with small clutches had
a significantly longer LA4, while females
with four egg clutches were significantly
larger than those with smaller or larger
clutches in weight, bill depth, and LA4.
Young from four egg clutches were also
Santa
Character Cruz Males Females All
G. fortis
WGT 1.00 .75 .51
WNG .98 .60 .79
TRS .96 .92 .72
BLG .99 .95 .98
BDT 1.00 .93 .96
BWD 1.00 .99 .98
LA4 .88 .59 .48
.73
.75
.91
.96
.94
.98
.59
.97
.84
.82
.77
N 10, 40 42, 90 9, 19 118, 246
G. scandens
WGT .84
WNG .58
.25
.62
.55
.62
TRS .97 .96
BLG .94 .76
BDT .94 .89
BWD .98 .95
.94
.80
.87
.95
.61
LA4
.67
.44
.85 .77 .76
N 14, 28 10, 20 36, 74
larger in weight, bill length, bill depth,
and bill width. Young showed no significant variation across numbers of young
fledged,
Thus G. fortis on the inner slopes in
1978 were larger than in other areas. Large
adults survived best in 1977 (Boag and
Grant, 1981), and birds breeding on the
inner slopes in 1976 survived especially
well (Boag, 1981). If inner slope territories
were also better for rearing young in 1978,
inner slope fortis should have shown increased breeding success. But inner slope
larger than young from larger or smaller
clutches, with significant differences for bill
nests were no more successful than nests
in other areas (Boag, 1981). Alternatively,
depth, width, and LA4. There was no sigif there was a strong territory quality efnificant variation in male size across numfect, inner slope young might have reached
bers of young fledged, while females fledga larger size relative to their parents than
ing four or more young were significantly
young raised elsewhere. Again, there was
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882
PETER
T.
BOAG
TABLE 2. Product moment correlations between G. fortis and G. scandens mates on Daphne in 1976, 1977,
and 1978. All pairs shown fledged one or more young. No G. fortis bred in 1977. Significance levels in this
and subsequent tables: *, P < .05; **, P < .01; * P < .001.
G
Character
WGT
-.06
BDT
40
1976
-.10
.19
.13
.28
23
.02
.09
no obvious tendency for this to be the case.
.24
.49*
-.32
.16
11
.41
-.16
.30
-.17
16
1978
-.39
-.15
-.42
-.04
-.32
1977
-.47
-.17
-.15
.41**
-.10
scandens
.24
-.15
.35*
LA4
1978
-.26
.30
BWD
G
-.15
.38*
BLG
N
1976
.14
WNG
TRS
fortis
-.24
-.11
20
new averages for birds remeasured since
Thus large parents did produce large young
1976. The revised data support the origi-
in the inner slope area, but this does not
nal conclusion of significant assortative
seem to have been augmented by a cor-
mating for some characters in 1976fortis,
relation between large parents and supe-
but a comparison of correlations in suc-
rior breeding resources.
cessful and unsuccessful 1976 pairs (Sokal
and Rohlf, 1969) showed no significant
Correlations Between Mates
difference between the two groups. I also
Boag and Grant (1978) showed that the
used canonical correlation to simulta-
morphology of 1976 G. fortis mates was
neously examine all the characters in
correlated, especially in successful pairs.
groups of male and female mates; again
Table 2 summarizes correlations between
only the results for the successful 1976for-
mates fledging at least one young. The 1976
tis sample approached significance (R2 =
fortis values have been recalculated, using
.62, X249= 58.01, P = .18; P values for
TABLE 3. Pooled 1976 and 1978 G. fortis heritabilities, followed by averages for separate 1976 and 1978
estimates. Presented as h2 + SE, based on family size weighted regressions of offspring means on their
midparents, male parents, andfemale parents, and intraclass correlations amongfull sibs. N is the number
of family groups followed by the total number of offspring involved. Significance levels are those of the
corresponding regression or analysis of variance.
Character
Midparent
Male
Female
Sib
Pooled
WGT .91 + .09*** .95 ? .22*** .81 ?.17*** .78 ? .19***
WNG .84 ? .14*** .82 ? .24*** .61 ?.17*** .42 ? .20*
TRS
.71
.10***
.61
?
.19**
.61
?
.13***
.32
?
.20*
BLG .65 + .15*** .75 ? .27** .92 ? .17*** 1.11 ? .17***
BDT .79 ? .09*** 1.03 ? .19*** .87 + .15*** 1.12 ? .17***
BWD .90 + .10*** 1.02 ? .22*** .96 ? .17*** .99 ? .18***
LA4
.35
?
.10**
.55
?
.74
N
39,
82
46,
.18**
.37
.82
85
57,
?
.14**
.74
111
.64
?
.20***
.77
46,
129
1976
.75
N
22,
26
N
17,
56
34,
.82
44
.77
32,
37
.87
18,
38
1978
.72
12,
.77
41
.71
25,
74
.71
28,
91
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FINCH
other samples were ?. 90). This suggests
HERITABILITIES
I11.0-
* 0
that the assortative mating in even this
group is relatively weak overall. Table 2
shows that this correlation is not present
at all in another year (1978) or species
1978
E
y
0.74x+2.50
r=
there were no significant differences between 1976 and 1978 except for tarsus in
the male-offspring regression (t-test of 1976
versus 1978 tarsus regression slopes, t =
2.20, df. = 80, P < .05). The absence of
0 9
m0 0 - 1976
Geospiza fortis Heritabilities
lar, and when compared prior to pooling,
0
63%
0
heritabilities in 1976 and 1978 were simi-
0
-C 2~~~~~~~
10.0-
(scandens).
Table 3 shows that average G. fortis
883
O / O 04 y= 0.82x+ 1.27
a
9.0
.0
58
0
cn
0'
/
oo
0~~~~
8.0- '
'0
8.0
0
9.0
10.0
11.0
Midparent Bill Depth (mm)
inflated female-offspring heritabilities
FIG. 1. Regressions of G. fortis mean offspring
suggests that maternal effects are mini-
bill depth on midparent bill depth in 1976 (open cir-
mal. More surprisingly, average full sib
estimates are also only slightly larger than
cles) and 1978 (solid circles). See also Table 3. The
slopes of the lines are not significantly different, but
analysis of covariance showed that the 1978 line has
other estimates, suggesting that common
a significantly higher Y-intercept. Crosses indicate
environment and nonadditive genetic ef-
bivariate means.
fects are also not very important in this
population. Taken individually or pooled,
the two years' data suggest that about 76%
of the phenotypic variation in external
morphology of G. fortis is heritable.
relatively larger young were produced in
1978. Table 4 compares means for the two
Despite the similarity of the two years'
years, showing that the main effect is a
results, the small differences may be of
depression of offspring size in 1976. The
biological interest. For instance, 1976 single parent regression heritabilities were
small size of 1976 young appeared per-
larger than in 1978, as expected given the
and remeasured the next year showed no
weak assortative mating observed in 1976
(Falconer, 1981). Full sib heritabilities
tively smaller young in 1976 presumably
were also larger in 1976, again expected if
interfamily variation was increased by
density dependent environmental effects,
as discussed below.
Environmental Effects
Analysis of covariance showed that
while midparent-offspring regression
slopes were similar in the two years, yintercepts were greater in 1978, signifi-
cantly so for tarsus (P < .05), bill depth
(P < .01), and LA4 (P < .01). Figure 1
illustrates this for bill depth; the 1978 data
are shifted to the right because 1978 parents were larger than 1976 parents due to
manent, as 10 young measured in 1976
evidence of "catch-up growth." The relaresulted from poor conditions for growth
that year, due to high breeding densities,
later reduced by the 1977 drought on
Daphne (Boag and Grant, 1981). Thus in
January 1976 thefortis population size was
1144, with territories (x7 ? SE) of 203.6 +
18.9 'm2 (N = 19), while in January 1978
the population size was 181, with territo-
ries of 477.8 ? 55.0 m2 (N = 9). It is also
worth noting that the homogeneity of these
regression slopes in the face of the different environments of 1976 and 1978 argues
against the presence of genotype-environment interactions (Falconer, 198 1).
natural selection (Boag and Grant, 1981),
Uncertain Paternity
and the points are shifted upwards both
because of the larger parents and because
1978 data using males seen to rear off-
Regressions originally calculated for the
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884
PETER
T.
BOAG
TABLE 4. Means (x) and coefficients of variation (CV = 100 x SD/x) for G. fortis parents and offspring
used in 1976 and 1978 midparent-offspring h2 analyses (Table 3). Adult statistics are based on equal numbers
of males andfemales making up midparents, and thus the CVs are based on the total parental variance, not
the variance of midparent values. PC1 scores are discussed in the text, and are based on the rp PCA in Table
8. The PC scores are standardized, and thus variances are given here instead of CVs, to indicate how the
various subsamples depart from the overall variance of 1.0.
1976
Adults
Character
WGT
15.86
WNG
TRS
x
8.05
68.09
1978
Offspring
CV
15.05
3.48
x
Adults
CV
10.15
66.15
3.79
x
16.75
69.09
Offspring
CV
x
CV
9.68
16.48
9.21
3.33
67.95
2.85
3.57
18.75
3.42
18.58
3.53
19.08
3.80
19.09
BLG
10.74
6.64
10.35
8.13
11.04
5.55
10.83
6.31
BDT
9.56
9.29
8.96
9.12
9.90
8.62
9.88
6.79
BWD
LA4
8.74
3.56
PC1
.03
N
6.66
9.25
.97
8.45
3.68
-.69
44
7.72
8.49
1.31
26
spring gave low heritabilities (average h2
for the seven characters in the 22 original
1978 male-offspring families was .35).
8.95
3.46
.57
6.94
8.89
6.13
9.96
3.41
6.66
1.14
34
.39
.78
58
same parents were pooled. To justify the
pooling, eight G. fortis females were selected which had produced multiple broods
High heritabilities were obtained in 1978
with the same male, and for which I had
using other methods, suggesting either that
recaptured and measured at least two off-
strong maternal or nest environment effects were present, or that 1978 paternities
spring from two or more broods. ANOVA
were uncertain. There were behavioral and
breeding data to support the last alternative. 1976 G. fortis pairs each raised only
one clutch, whereas 1978 fortis females
produced three clutches (Boag, 1981). In
24% of the 1978 renestings, females left a
nents, showing that the variance between
territory for a new male, sometimes before
her brood had fledged, leaving the first
male to rear those young. In several cases
the female left her first mate and laid in
the nest of a new male in less than a week,
suggesting that some eggs could have been
fertilized by the original male. Thus I used
the relatively small sample of faithful pairs
and their broods to produce the 1978 maleoffspring heritabilities in Table 3, despite
large standard errors. In other analyses
uncertain paternity is less important and
a conservative revision of parentage was
used to add several families to the known
was used to calculate variance compobroods was not significant for any char-
acter (mean component for the seven char-
acters was 6.7%), with the relative sizes
of the among females components (44.4%)
and within broods components (48.9%)
determining the heritabilities of the traits.
Young in successive broods did of course
have highly significantly different ages; the
absence of significant between brood morphological variance components confirms
that excluding young under eight weeks
old minimized differences in morphology
due to age.
Geospiza scandens Heritabilities
Heritabilities were calculated in a similar fashion for the combined 1976 and
1978 G. scandens sample discussed in the
Methods. Table 5 shows several differ-
1978 faithful pairs, based on nest chron-
ences from the G. fortis data. Less than
ologies and behavioral observations.
half of the phenotypic variance in scan-
Differences Between Broods
Because 1978 pairs produced several
clutches, fully grown young having the
dens morphology is heritable on average,
and the rankings of the average heritabilities for the seven characters do not match
those of fortis (Spearman correlation, r, =
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FINCH
HERITABILITIES
885
TABLE 5. G. scandens heritabilities, combining 1978 data with four 1976 families. Presented as h2 ? SE.
N is the number offamily groups followed by the total number of offspring.
Character
WGT
.58
WNG
.12
Midparent
Male
Female
Sib
+
.39
.37
?
.32
.14
+
.58
.35
?
.39
?
.26
.11
?
.42
.19
?
.42
.35
?
.39
TRS .92 ? .23*** 1.26 ? .36*** .94 + .39* .88 ? .35**
BLG
.32
BDT
.14
BWD
LA4
?
.34
.60
It
N
?.24
+
1.29
.32
?
.02
.42
.20**
29
?
.44
.62
.43
16,
?.30***
?
.37
?.41
-.18
.22***
.59
20,
.04
-.01
35
-.23; here and subsequently, significance
?
?
.39
.45
.56
?
.39
?.70
.56
?
.39
?
-.17
.33
?.34
.18
20,
.30
34
.06
+
.38
.44
15,
38
1980; Grant, 198 la) and warrants further
study.
levels of r, are omitted because of lack
of
independence). Geospiza scandens females
also switched mates in 1978, but herita-
Correlations Between Characters
bilities and nest chronologies suggested that
Phenotypic, genetic, and environmental
few of the scandens families involved
correlation matrices for G. fortis are shown
young of uncertain paternity. Some of the
in Table 6. The genetic correlations for
reduction in the heritabilities of scandens
fortis are high, so that the environmental
reflects lower repeatabilities in this species;
correlations are largely "residuals" (Lea-
note particularly that scandens females
my, 1977). Separate analyses of the 1976
display low repeatabilities and low herita-
and 1978 fortis data sets did, however,
bilities. The only consistently high scandens heritability was for tarsus length,
show good overall matching of matrix elements for all three types of correlations
which had an intermediate value infortis.
(rank correlations between 1976 and 1978
Nestlings
It would simplify field work and in-
matrix elements: rp, r, = .92; rG, r, = .66;
rE, r, = .52). Table 6 shows there is also
good correspondence between the ele-
crease sample sizes in studies such as this
ments of the rp and rG matrices (r, = .8
if offspring could be measured before they
but no such similarity between the rE and
fledged. Unfortunately these methodolog-
either the rp (r, = .13) or rG (r, = -.12)
ical advantages are offset by theoretical
matrices.
difficulties in interpreting such data (Fal-
Phenotypic correlations were generally
coner, 1981). Nevertheless, some workers
lower in G. scandens (Tables 6 and 7; av-
have examined resemblance between fully
erage absolute value of rp infortis was .56
grown parents and their growing offspring
and in scandens .39). Geospiza scandens
had lower heritabilities, with larger stan-
(Brooke, 1977; Grant, 198 la). When I regressed the mean weight of 1978 fortis
dard errors, and this is reflected in the un-
young at banding (7 days old) on the weight
reliable genetic and environmental corre-
of their midparents, I found a slope of
lations shown in Table 7. They are
.61 + .28 (P < .05). Such a regression in-
presented largely to illustrate the sampling
corporates a type of cross-covariance, and
errors possible when rG is calculated from
with a proper estimate for "7 day weight"
small samples using low and imprecise
genetic variance could give a genetic co-
heritability estimates. While in fortis ge-
variance between "7 day" and "adult"
netic correlations are high compared to
weights (Falconer, 1981). Parent-off-
environmental correlations (average ab-
spring resemblance during ontogeny has
not received wide attention (Vandenburg
solute values, rG = .75; rE = .36), the reverse is true in scandens (rG = .45; rE =
.86) (Falconer, 1981).
and Falkner, 1965; Atchley and Rutledge,
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886
PETER
T.
BOAG
TABLE 6. Phenotypic, genetic and environmental correlation matrices for G. fortis. rp based on 1976 and
1978 pooled within group correlations, N = 275. All correlations have been multiplied by 102 and decimal
points omitted. Diagonal of rp matrix contains phenotypic standard deviations (log10) multipled by 102. rp
values > 12 are significant. Upper parts of rG and rE matrices contain standard errors. Diagonal of rG matrix
contains h2 values based on log1o scale.
WGT
WNG
TRS
BLG
BDT
BWD
LA4
rp
WGT 4.03
WNG
+64
TRS
+60
BLG
BDT
1.45
+56
1.59
+69 +60 +52 2.79
+76 +64 +54 +81
BWD +75 +60
LA4 -34 -27
+52
-20
3.64
+78
-12
+88 2.94
-46 -41
3.57
rG
WGT
.85
.10
.13
.10
.07
.07 .26
.11 .28
.17
.32
+ 95 + 95 +71 .67 .07 .08 .34
+87 +87 +75 +90 .82 .04 .23
WNG +88 .89 .15 .12 .10
TRS
+89
+68
.65
.18
.15
BLG
BDT
BWD +94 +78 +61 +89 +93 .90
LA4 -55 -30 -43 -48 -79 -70
.24
.39
WGT
.56
rE
3.11
WNG
-98
TRS
-26
BLG
BDT
BWD
LA4
1.06
1.02
1.03
.80
1.83
2.51
+21
.49
.76
-13
-68
.46
.64
.44
+19
-75
-02
+57
.73
.54
-97
+26
+47
+60
.75
-59
-07
-37
+15
2.69
3.68
.66
.79
.38
+02
+28
-04
+04
I extracted principal components from
ilar results from separate 1976 and 1978
the G. fortis rG and rE matrices for com-
analyses, suggests that environmental cor-
parison with the phenotypic PCA discussed below. Both matrices were ill-con-
are large and positive, like the phenotypic
relations among BLG, BDT, and BWD
ditioned for PCA, a not uncommon result
and genetic correlations among these
(Leamy, 1977; Arnold, 1981). BMDP
characters, while there are strong negative
(Dixon and Brown, 1979) did not accept
correlations between WGT or WNG and
either matrix, but SPSS (Nie et al., 1975)
did, as it calculates simple principal components without inverting the correlation
matrix. These admittedly strained analy-
most other characters. This hints at dif-
ses are shown in Table 8; the genetic correlations display a multivariate structure
similar to the phenotypic correlations,
while the environmental matrix has a different structure. This was confirmed by
cluster analyses of the correlation matrices
(BMDP1M, with average linkage, Dixon
ferent pathways of environmental covariation in these two groups of characters. WGT and WNG are likely to be
influenced by the condition of a bird (Table 1), reflecting recent, largely external
influences. Environmental covariation
among beak characters may more closely
reflect internal effects, active primarily
during periods of growth.
and Brown, 1979), an alternative to using
Heritabilities of Principal Components
PCA on ill-conditioned matrices (Leamy,
Table 8 shows unrotated PCs extracted
from rp matrices in Tables 6 and 7. In all
cases PCs 5 through 7 were not significant
1977).
The G. fortis rE matrix, backed by sim-
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FINCH
HERITABILITIES
887
TABLE 7. rp, rG and rE matrices for G. scandens, as in Table 6, with N = 92. rp values > 20 are significant.
WGT
WNG
TRS
BLG
BDT
BWD
LA4
rp
WGT 3.55
WNG
+66
TRS
+35
BLG
BDT
+36
+56
+44
BWD
LA4
1.40
+43
+04
1.52
+58 +11 2.04
+56 +47 +36
+51
+38
+39
+10
-40
+38
2.19
+75
-32
1.96
-14
3.44
rG
WGT .58
WNG +57
.44 .33 .7 9 .99 .59 .41
.25 .50 1.53 3.74 1.27 .64
TRS +99 +61 .94 .53 1.26 .52 .25
BLG -13 -48 -10 .32 3.23 1.02 .44
BDT +30 -82 +77 -90 .09 1.25 1.89
BWD +13 -33 -01 -27 +29 .35 .55
LA4 +10 -20 -66 +60 -102 +17 .83
rE
WGT
.41
9.00
.61
.43
.52
1.00
WNG
+79
1.21
.41
.34
.41
.94
TRS -235 +31 2.81 2.82 5.82 8.78
BLG +114 +100 +83 .38 .44 .72
BDT +60 +82 +106 +64 .30 .66
BWD +70 +87 +195 +72 +91 1.08
LA4 -11 +53 +174 +22 -13 -67
(Ricklefs and Travis, 1980). Heritabilities
were calculated for both species using the
same methods as before, applied to PC
scores. Table 8 shows that PC1, representing overall body size (Boag and Grant,
1981), was most strongly inherited in G.
fortis, while PC2, representing bill point-
edness, and PC3, representing a contrast
between bill and non-bill characters, were
most strongly inherited in scandens.
Response to Selection
The most important implication of high
heritabilities is the prediction that selec-
tion of G. fortis parents should result in a
corresponding shift in the phenotypes of
their offspring. Geospiza fortis underwent
strong directional natural selection on
Daphne between 1976 and 1978 (Boag and
Grant, 1981), and thus the data in Table
4 can be used to determine whether the
1978 offspring display the predicted re-
sponse. To test this, I standardized the
4). The 1978 parents displayed an average
increase in size of .44 SD due to selection,
while their offspring increased by .31 SD
relative to the 1976 midparents. The already standardized PC1 means show a
similar result; 1978 midparents were .54
SD larger, while their offspring showed a
response of .36 SD. In both cases the increase in the size of 1978 young relative to
the increase seen in their selected parents
is close to that predicted by heritabilities
of about 76% (Falconer, 1981). With larger sample sizes, these data could in principle be used to estimate realized heritabilities (h2r) (Falconer, 1981), although a
multivariate generalization of the formula
given at the beginning of this paper would
be required to cope with the complexities
of natural selection acting on correlated
characters (i.e., A = GP-1S as opposed
to R = h2S; see Lande, 1979).
DISCUSSION
1978 midparent and offspring means with
These data support the conclusions of
respect to the means and standard devia-
Boag and Grant (1978), namely that external morphology is strongly heritable in
tions (SD) of the 1976 midparents (Table
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888
PETER
T.
BOAG
TABLE 8. Unrotated PC loadings for G. fortis rp,
natural populations of Darwin's finches.
rG and rE matrices, and for G. scandens rp matrix.
Geospiza fortis has particularly high her-
EIG are eigenvalues, while % V is the percent of the
itabilities for weight and bill dimensions,
total phenotypic variance explained by each PC.
Heritabilities of each PC, together with their standard errors and significance levels, are given below
the fortis and scandens rp PCAs. The h2 estimates
are based on PC scores used in the midparent-offspring regressions of Tables 3 and 5.
and for overall body size as represented
by PC1. Results for G. scandens are less
complete, but suggest that heritabilities are
lower in this species, and that in contrast
to fortis, the highest heritabilities are for
tarsus length and shape PCs 2 and 3.
Character
PC1
PC2
PC3
PC4
WGT
.87
WNG
TRS
.71
BLG
.04
.78
.85
BDT
corresponds in part to high repeatabilities.
.55
Garnett (1976) reported repeatabilities
-.59
-.32
.29
-.04
higher than my long term values, but his
.22
-.05
.26
-.09
for much growth, molt, abrasion or change
in measurement technique to take place.
-.09
.91
-.05
-.25
.31
.93
BWD
-.02
.12
.21
The heritabilities of G. fortis are high
compared to other birds (Table 9) and this
G. fortis, rp
-.06
data were collected over too short a period
LA4
-.45
.88
.11
.01
EIG
4.48
.93
.62
.42
Smith and Zach's (1979) study is more
%
63.9
13.3
8.8
6.0
comparable, and their repeatabilities were
V
h2 .75*** .36** .47** .32**
SE
.12
.10
.15
.10
G. fortis, rG
WGT
.98
.13
-.10
WNG
.89
.37
.21
-.18
-.56
-.02
TRS
.81
BLG
.19
.95
BDT
.98
BWD
.19
.17
-.17
.94
.19
.01
.06
-.15
lection (Falconer, 1981). If female choice
-.66
.75
.07
.06
.84
.44
.16
%
80.1
12.0
6.3
2.2
G. fortis, rE
WGT .28 -1.00 -.02 .36
WNG -1.06 .38 -.04 -.05
.01
.59
.01
.75
.28
.19
BDT
.82
BWD
LA4
EIG
.00
-.33
for other reasons. The mean dimensions
of young produced in different years may
differ (Table 4, Fig. 1), because of changes
-.20
-.17
.94
-.05
1.08
.82
% V 44.8 27.2 15.4 11.6
G. scandens, rp
WNG
.83
TRS
.59
BLG
.65
BDT
.82
BWD
LA4
EIG
%
V
.23
.37
-.36
.24
.15
-.09
-.51
.59
-.31
.44
.44
-.02
-.34
.11
-.04
.79
-.15
-.48
.10
-.10
.90
-.06
.30
3.35
1.65
.69
47.9
23.6
9.9
.45
6.4
h2 .20 1.07*** .64** -.09
SE
.39
.20
.22
1981). This was not observed, suggesting
.01
.57
.77
of an excess of males (Boag and Grant,
-.03
.05
WGT
mation of many new pairs in the presence
.81
.80
1.90
mate correlations, one would predict
higher correlations in 1978 due to the for-
that the 1976 pairs were weakly correlated
.27
3.14
Correlations between mates affect heritability estimates and the response to se-
had been responsible for the 1976 G. fortis
5.61
BLG
plain the lower scandens heritabilities.
.22
EIG
TRS
are lower in scandens, particularly scandens females, but do not completely ex-
-.19
.20
LA4
V
lower. Repeatabilities for some characters
.30
in nestling food availability, and because
selection alters parental phenotypes. Perhaps after several years of regular recruitment to the breeding population, pairs
composed of a male and female reared in
the same year may gradually accumulate,
inducing a correlation into the overall
breeding population. Van Noordwijk et al.
(unpubl.) reported no correlations between great tit mates, while Smith and
Zach (1979) noted only one significant,
negative, correlation between song sparrow mates.
The male-offspring heritabilities in 1978
fortis were complicated by uncertain pa-
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FINCH
HERITABILITIES
889
TABLE 9. Heritabilities of avian external morphology. Data for G. fortis are pooled midparent values from
Tables 3 and 8, while G. scandens data are midparent values from Tables 5 and 8.
Species WGT WNG TRS BLG BDT BWD PC 1 Reference
Puffinus puffinus .661 .92 .761 .92 Brooke, 1977
Ficedula hypoleuca - - .5 7 - .5 7 Alatalo et al., unpubl.
F. albicollis - - .59 - .59 Alatalo et al., unpubl.
Parus major - - .52 - .52 Alatalo et al., unpubl.
P. major .59 - .5 2 - .56 Van Noordwijk et al.,
1980, unpubl.
P. major - .76 .76 Garnett, 1981
P. major - - .62 - .62 Dhondt, 1982
Melospiza melodia .04 .14 .32 .33 .51 .50 - .31 Smith and Zach, 1979
Geospizafortis .91 .84 .71 .65 .79 .90 .75 .79 Present study
G. scandens .58 .12 .92 .32 .14 .60 .20 .41 Present study
G. conirostris 951 -.681 .87 .481 .661 741 - .87 Grant, 1981a
Branta canadensis .20 - .15 .53 - .29 Lessells, 1982
1 Character unlikely to have been fully grown in offspring measured, a
ternity. Mis-directed parental care may
ance implied by high heritabilities is main-
lead to selection for behavior to ensure pa-
tained. Grant and Price (1981) discuss this
ternity (Fujioka and Yamagishi, 198 1), but
problem in detail, and here I review only
evaluation of paternity in natural popu-
those arguments specific to Daphne.
lations is difficult without elaborate ex-
The level of variation in a population is
periments (Bray et al., 1975) or genetic
markers (Mineau and Cooke, 1979). I tried,
largely a function of mutation, genetic
drift, migration, and selection (Falconer,
1981). Lande (1975) suggests that muta-
with little success, to identify the paternity
of questionable broods by examining the
residuals of heritability regressions. How-
maintain substantial amounts of polygenic
ever, in studies with larger sample sizes,
variation, but it is difficult to see why they
outlier tests (Sokal and Rohlf, 1969) on
male-offspring regressions may help as-
should be more effective in Daphnefortis
sess paternity.
My results suggest that body size and
tion and recombination may be able to
compared to closely related species, i.e.,
scandens. Minimum annual population
sizes for Daphne finches are available for
bill dimensions ought to be especially re-
seven years (Boag, 1981), and suggest that
sponsive to natural selection in G. fortis.
This is important, because considerable
the effective population size (Ne) of fortis
is no more than 460, while Ne for scan-
effort has been devoted to studying the
dens may be about 230. Skewed sex ratios
evolutionary and functional relationships
in years such as 1978 (Boag and Grant,
between variation in bill or body size, and
the feeding ecology, adaptive radiation and
120' and 80, respectively (Falconer, 1981).
1981) could reduce Ne to values as low as
species recognition of Darwin's finches
Thus genetic drift, if anything, should re-
(Lack, 1947; Bowman, 1961; Grant et al.,
duce variation in both species, albeit more
1976; Abbott et al., 1977; Boag and Grant,
so in scandens.
1981; Grant, 198lb; Ratcliffe, 1981). It has
There is introgression between Daphne
also been suggested that intraspecific vari-
G. fortis and small ground finch (G. fuli-
ation itself may be maintained by natural
selection (Grant et al., 1976; Smith and
Zach, 1979). As with biochemical varia-
ginosa) immigrants at an annual rate of
tion, the major problem is to explain how
immigrants from Isla Santa Cruz (Boag,
the large amount of additive genetic vari-
1981). Thus migration explains in part how
1. 1% to 3.5%; Daphnefortis probably also
mate with morphologically distinct fortis
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890
PETER
T.
BOAG
large Daphnefortis heritabilities might be
as Santa Cruz, spatially varying selection
maintained (Grant and Price, 1981). How-
pressures may actually promote variation
ever the effect of selection regime on ge-
in fortis (Grant et al., 1976). Unfortu-
netic variability is a matter for more de-
nately, present theoretical models do not
bate. There is little doubt that stabilizing
adequately describe situations such as
selection reduces variation, but the effect
these. On Daphne, thefortis population is
of different types of directional selection
probably not often at genetic equilibrium,
on variation remains uncertain (Grant and
population dynamics are unpredictable,
and selection pressures may change in direction and intensity from season to season
and from year to year, with strong density
and frequency dependent effects likely to
be the rule rather than the exception
(Clarke, 197 9).
Another aspect of the uncertain rela-
Price, 1981).
Current data suggest that Daphne G.
fortis are subject to temporally fluctuating
directional selection on morphology, while
scandens experience stabilizing selection
(Grant et al., 1976; Boag, 1981; Boag and
Grant, 1981; Grant and Price, 1981). The
selection regimes of the species reflect their
ecologies; Daphnefortis are opportunistic
generalists, experiencing large population
fluctuations and phenotypic shifts as rainfall alters seed abundances and sizes (Boag
and Grant, 1981). When food is short, intraspecific competition among fortis appears intense, and diets expand, while intraspecific correlations between
morphology and diet (Boag and Grant,
tionship between selection and heritability
is the paradox that in quantitative genetics, small heritabilities are associated
with traits closely related to fitness (Falconer, 1981). The assumption is that fitness or "major fitness components" are
continually subjected to unidirectional selection, eliminating additive genetic vari-
ance. In nature it is usually difficult to find
or measure a "major fitness component."
1981; Grant, 198 lb) imply that selection is
Even characters such as clutch size in birds
likely to be frequency dependent. Geospiza scandens experience less violent population changes because their specialized
occupy intermediate optima and display
significant amounts of heritable variation
(van Noordwijk et al., 1980). This is
because selection can reduce VA in total
fitness, while at the same time pressures on
individual components (e.g., clutch size)
feeding and breeding ecology (Lack, 1947;
Boag, 1981) buffers them against changes
in food availability. In periods of food
shortage scandens diets contract and interspecific competition with fortis predominates (Boag, 1981); there is no evidence for intraspecific correlations between
morphology and diet in scandens.
Theory predicts that fluctuating directional selection is unlikely to maintain genetic variation unless selection pressures
vary spatially and not just temporally
(Grant and Price, 1981). Despite this prediction, Mackay (1980) found that temporally varying directional selection maintained higher heritabilities in laboratory
populations of Drosophila than did spatially varying selection. Thus the selection
regimes currently seen on Daphne would
reduce additive genetic variance in scandens, and might at least slow the loss of
variation infortis. On larger islands, such
cancel as negative genetic correlations are
established between characters coupled to
fitness by different mechanisms (Falconer,
1981).
As quantitative genetic theory is integrated into evolutionary ecology, genetic,
especially negative genetic, correlations
will be the focus of much interest. Given
the prevalence of pleiotropy, the evolution
of almost any character is constrained or
assisted by selection on a host of other
characters; natural selection is always for
"fitness," so that all observed phenotypic
responses are in some sense correlated responses. This will apply to morphology
(Lande, 1979; Atchley et al., 1981), reproductive characteristics (Lande, 1982), food
preferences (Arnold, 1981), or even the
complex behavioral "trade-offs" of forag-
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FINCH
HERITABILITIES
891
ing theory (McCleery, 1978). Before much
imize complications found in natural
progress can be made in such areas, it will
populations, such as genotype-environ-
be necessary to adapt quantitative genetic
ment correlations, assortative mating, and
theory to situations governed chiefly by
natural selection. Such an approach is ca-
natural selection operating on correlated
pable of precise results, but lest carefully
characters (Lande, 1979). One serious
controlled experiments become ends in
methodological problem is the notorious
themselves, a constant effort must be made
unreliability of genetic correlations; in some
to test their generality and realism in field
cases, reasonable estimates of rG may re-
situations (Levins, 1968). I suggest that
quire 1,000+ parent-offspring pairs (Van
neither uncontrolled studies of natural
Vleck and Henderson, 1961). A presum-
populations nor elegant studies of labo-
ably worse problem holds true for rE, al-
ratory organisms alone will in the long run
though less attention has been paid to its
answer the question of how polygenically
sampling variance (Cheverud, 1982).
determined phenotypes evolve in response
Another point other workers should
to changing environments. Given this
consider is that despite the strong genetic
premise and the pressure for more rigor-
influence, the environment did signifi-
cantly affect finch morphology on Daphne,
ous evolutionary explanations of phenotypic patterns (Gould and Lewontin, 1979),
primarily by reducing the mean size of off-
it remains surprising that there have been
spring in a poor year. Nutritional condi-
no parallel collections of quantitative ge-
tions can alter the growth rates of nest-
netic data from natural and controlled
lings (Bryant, 1978), but no attention has
laboratory populations of any single avian
been paid to whether such effects produce
species, using characters of ecological im-
smaller adult birds; i.e., there is little in-
portance and which historically have been
formation on canalization or "norms of re-
assigned high adaptive values.
action" for avian morphological characters. Such information is important
SUMMARY
because selection acts on phenotypes. Even
The repeatabilities of seven external
if heritabilities within a single population
morphological characters were high for
and year are high, nutritional effects on
Geospiza fortis and G. scandens on Isla
the mean or variance of body size among
Daphne Major, Galapagos, between 1975
fledglings could cloud the evolutionary
and 1978. Geospizafortis mates displayed
significance of the high, sometimes selec-
positive assortative mating with respect to
tive, first year mortality seen in many birds
morphology in 1976, but not 1978, while
(Johnston and Fleischer, 1981; van
scandens showed no consistent assortative
Noordwijk et al., unpubl.). Also, most of
mating in any year. Heritabilities infortis
the populations in Table 9 are sedentary,
were high in both years, averaging .76
based on three types of parent-offspring
largely because sedentary or strongly phil-
opatric species are chosen for long term
regression and on full sib intraclass cor-
population studies. In other species, local
relations. Heritabilities in scandens were
breeding populations may be composed of
lower, averaging .46. 1978 heritabilities
birds reared in a variety of other, some-
were complicated by uncertain paternity
in some fortis families. Genetic correla-
times distant populations. If environmental effects produce locally unique devia-
tions were also high among the seven
tions in offspring phenotypes, such mixed
characters in fortis, and had a multivari-
breeding populations would display in-
ate structure like that seen in the phenotypic correlations. Geospiza fortis had a
creased environmental variances and decreased heritabilities.
Individual philosophies differ (Kemp-
thorne, 1977 p. 3), but quantitative geneticists have traditionally sought to min-
high heritability for PC1, representing
overall body size (h2 = .75), while scandens had high heritabilities for PC2, representing bill "pointedness" (1.07), and
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892
PETER
T.
BOAG
PC3, representing a ratio between bill and
non-bill characters (.64). As predicted by
the heritabilities, fortis offspring showed
a strong phenotypic response to natural
selection of their parents in 1977. Geospiza
fortis morphological variation may be influenced by introgression with G. fuliginosa and frequency dependent, tempo-
rally fluctuating directional selection, while
G. scandens morphology may reflect an
evolutionary history predominated by stabilizing selection.
of floristic diversity and interspecific competition.
Ecol. Monogr. 47:151-184.
ARNOLD, S. J. 1981. Behavioral variation in natural populations. I. Phenotypic, genetic, and environmental correlations between chemorecep-
tive responses to prey in the garter snake,
Thamnophis elegans. Evolution 35:489-509.
ATCHLEY, W. R., ANDJ. J. RUTLEDGE. 1980. Genetic components of size and shape. I. Dynamics
of components of phenotypic variability and covariability during ontogeny in the laboratory rat.
Evolution 34:1161-1173.
ATCHLEY, W. R., J. J. RUTLEDGE, AND D. E. CowLEY. 1981. Genetic components of size and
shape. II. Multivariate covariance patterns in the
rat and mouse skull. Evolution 35:1037-1055.
BECKER, W. A. 1975. A Manual of Quantitative
ACKNOWLEDGMENTS
The data were collected while I was a
graduate student in the Department of Bi-
Genetics. Students Book Corp., Pullman.
BERRY, R. J. 1977. Inheritance and Natural History. Collins, London.
BOAG, P. T. 1981. Morphological variation in the
ology at McGill University, with financial
Darwin's finches (Geospizinae) of Daphne Major
support from a National Science and Engineering Council of Canada (NSERC)
Island, Galapagos. Ph.D. thesis, McGill Univ.,
scholarship, an NSERC operating grant
to P. R. Grant, and a travel grant from
the Frank M. Chapman Fund of the
American Museum of Natural History.
While the paper was written, I was sup-
Montreal.
BOAG, P. T., AND P. R. GRANT. 1978. Heritability
of external morphology in Darwin's finches. Nature 274:793-794.
1981. Intense natural selection on a pop-
ulation of Darwin's finches (Geospizinae) in the
Galapagos. Science 2 14:82-85.
ported by grants from the Trent Univer-
BOWMAN, R. I. 1961. Morphological differentiation and adaptation in the Galapagos finches.
sity research committee. I thank the
Charles Darwin Research Station (CDRS)
BRAY, 0. E., J. J. KENNELLY, AND J. L. GUARINO.
and the Ecuadorean Government for their
assistance in the Galapagos, particularly
CDRS directors C. MacFarland and H.
Hoeck, and national park intendente M.
Cifuentes. P. R. Grant, B. R. Grant, L.
M. Ratcliffe, E. Green, D. Nakashima,
Univ. Calif. Publ. Zool. 58:1-326.
1975. Fertility of eggs produced on territories of
vasectomized red-winged blackbirds. Wilson Bull.
87:187-195.
BROOKE, M. DE L. 1977. The breeding biology of
the Manx Shearwater. Ph.D. thesis, Univ. Oxford, Oxford.
BRYANT, D. M. 1978. Environmental influences
and B. Tompkins helped with fieldwork.
on growth and survival of nestling house martins
Delichon urbica. Ibis 120:271-283.
P. Kuo, T. Buelow, and P. Northrup
CARSON, H. L. 1976. Genetic differences between
helped with computing at Trent. I thank
R. Alatalo, L. Gustafsson and A. Lund-
CHEVERUD, J. M. 1981. Variation in highly and
berg, as well as A. J. van Noordwijk, for
permission to cite unpublished work.
Comments by P. R. Grant, K. Sittman,
G. Bell, L. M. Ratcliffe, T. D. Price, R.
Lande, J. Hegmann, M. G. Bulmer, A. J.
van Noordwijk, and D. S. Falconer and
his colleagues greatly improved the manuscript.
LITERATURE CITED
ABBOTT,I.,L. K. ABBOTT, ANDP. R. GRANT. 1977.
Comparative ecology of Galapagos ground finches (Geospiza Gould): evaluation of the importance
newly formed species. BioScience 26:700-701.
lowly heritable morphological traits among social
groups of rhesus macaques (Macaca mulatta) on
Cayo Santiago. Evolution 35:75-83.
1982. Phenotypic, genetic, and environ-
mental morphological integration in the cranium.
Evolution 36:499-516.
CLARKE, B. C. 1979. The evolution of genetic diversity. Proc. Roy. Soc. London B 205:453-474.
DHONDT, A. A. 1982. Heritability of blue tit tarsus
length from normal and cross-fostered broods.
Evolution 36:418-419.
DHONDT, A. A., R. EYCKERMAN, AND J. HUBLE.
1979. Will great tits become little tits? Biol. J.
Linn. Soc. 11:289-294.
DIXON, W. J., AND M. B. BROWN (eds.). 1979.
BMDP-79. Biomedical Computer Programs
P-Series. Univ. Calif. Press, Berkeley.
This content downloaded from 132.174.254.72 on Mon, 06 Mar 2017 15:40:15 UTC
All use subject to http://about.jstor.org/terms
FINCH
FALCONER, D. S. 1981. Introduction to Quantitative Genetics, 2nd ed. Longman, London.
. 1963. Quantitative inheritance, p. 193-216.
HERITABILITIES
893
quences of family size in the Canada Goose Branta canadensis. Ph.D. thesis, Univ. Oxford, Oxford.
In W. J. Burdette (ed.), Methodology in Mam-
LEVINS, R. 1968. Evolution in Changing Environ-
malian Genetics. Holden-Day Inc., San Francis-
ments. Princeton Univ. Press, Princeton.
LONG, T. 1974. The role of heritability in adjust-
co.
FELDMAN, M. W., AND R. C. LEWONTIN. 1975.
The heritability hang-up. Science 190:1163-1168.
ing phenotypic variability. Amer. Natur. 108:140142.
FuJIoKA, M., AND S. YAMAGISHI. 1981. Extra-
MACKAY, T. F. C. 1980. Genetic variance, fitness,
marital and pair copulations in the cattle egret.
and homeostasis in varying environments: an ex-
Auk 98:134-144.
perimental check on the theory. Evolution 34:
GARNETT, M. C. 1976. Some aspects of body size
1219-1222.
in the great tit. Ph.D. thesis, Univ. Oxford, Ox-
MCCLEERY, R. H. 1978. Optimal behavioural se-
ford.
quences and decision making, p. 377-410. In J.
R. Krebs and N. B. Davies (eds.), Behavioural
Ecology. Blackwell Scientific, Oxford.
MINEAU, P., AND F. COOKE. 1979. Rape in the
lesser snow goose. Behaviour 70:280-291.
NEVO, E. 1978. Genetic variation in natural populations: patterns and theory. Theoret. Pop. Biol.
. 1981. Body size, its heritability and influ-
ence on juvenile survival among great tits Parus
major. Ibis 123:31-41.
GOULD, S. J., AND R. C. LEWONTIN. 1979. The
spandrels of San Marco and the Panglossian par-
adigm: a critique of the adaptationist programme. Proc. Roy. Soc. London B 205:581-598.
GRANT, P. R. 1981a. Patterns of growth in Darwin's finches. Proc. Roy. Soc. London B 212:
403-432.
1981b. Speciation and the adaptive radiation of Darwin's finches. Amer. Sci. 69:653-663.
GRANT, P. R., B. R. GRANT, J. N. M. SMITH, I. J.
ABBOTT, AND L. K. ABBOTT. 1976. Darwin's
finches: population variation and natural selection. Proc. Nat. Acad. Sci. USA 73:257-261.
GRANT, P. R., ANDT. D. PRICE. 1981. Population
variation in continuously varying traits as an eco-
13:121-177.
NIE, N. H., C. H. HULL, J. G. JENKINS, K. STEINBRENNER, AND D. H. BENT. 1975. SPSS: Statistical Package for the Social Sciences. McGrawHill, N.Y.
VAN NOORDWIJK, A. J., J. H. VAN BALEN, AND W.
SCHARLOO. 1980. Heritability of ecologically
important traits in the great tit, Parus major.
Ardea 68:193-203.
O'DONALD, P. 1973. A further analysis of Bum-
pus' data: the intensity of natural selection. Evolution 27:398-404.
logical genetics problem. Amer. Zool. 2 1:795-81 1.
OJANEN, M., M. ORELL, AND R. A. VAISANEN.
GREENWOOD, P. J., P. H. HARVEY, AND C. M. PER-
1979. Role of heredity in egg size variation in
the great tit Parus major and the pied flycatcher
Ficedula hypoleuca. Ornis Scand. 10:22-28.
PATTON, J. L., S. V. YANG, AND P. MYERS. 1975.
Genetic and morphologic divergence among in-
RINS. 1979. The role of dispersal in the great
tit (Parus major): the causes, consequences, and
heritability of natal dispersal. J. Anim. Ecol. 48:
123-142.
JOHNSTON, R. F., AND R. C. FLEISCHER. 1981.
troduced rat populations (Rattus rattus) of the
Overwinter mortality and sexual size dimorphism
Galapagos archipelago, Ecuador. Syst. Zool. 24:
in the house sparrow. Auk 98:503-511.
296-310.
KEMPTHORNE, 0. (ed.). 1960. Biometrical Genetics. Pergamon Press, London.
. 1977. Introduction, p. 3-18. In E. Pollak, 0. Kempthorne, and T. B. Bailey, Jr. (eds.),
Proc. of the Internat. Conf. on Quantitative Genetics (1976). Iowa State Univ. Press, Ames.
KOLATA, G. B. 1974. Population genetics: reevaluation of genetic variation. Science 184:452-454.
LACK, D. 1947. Darwin's finches. Cambridge Univ.
Press, Cambridge.
LANDE, R. 1975. The maintenance of genetic variability by mutation in a polygenic character with
linked loci. Genet. Res. 26:22 1-235.
1979. Quantitative genetic analysis of
multivariate evolution, applied to brain: body size
allometry. Evolution 33:402-416.
1982. A quantitative genetic theory of life
history evolution. Ecology 63:607-615.
PERRINS, C. M., AND P. J. JONES. 1974. The in-
heritance of clutch-size in the great tit Parus major L. Condor 76:225-229.
POWELL, J. R., AND C. E. TAYLOR. 1979. Genetic
variation in ecologically diverse environments.
Amer. Sci. 67:590-596.
RATCLIFFE, L. M. 1981. Species recognition in
Darwin's ground finches (Geospiza, Gould). Ph.D.
thesis, McGill Univ., Montreal.
REEVE, E. C. R. 1955. The variance of the genetic
correlation coefficient. Biometrics 11:357-374.
RICKLEFS, R. E., AND S. PETERS. 1981. Parental
components of variance in growth rate and body
size of nestling European starlings (Sturnus vul-
garis) in eastern Pennsylvania. Auk 98:39-48.
RICKLEFS, R. E., AND J. TRAVIS. 1980. A mor-
phological approach to the study of avian community organization. Auk 97:321-338.
LEAMY, L. 1977. Genetic and environmental cor-
RISING, D., AND G. F. SHIELDS. 1980. Chromo-
relations of morphometric traits in randombred
somal and morphological correlates in two New
World sparrows (Emberizidae). Evolution 34:654-
house mice. Evolution 31:357-369.
LESSELLS, C. M. 1982. Some causes and conse-
662.
This content downloaded from 132.174.254.72 on Mon, 06 Mar 2017 15:40:15 UTC
All use subject to http://about.jstor.org/terms
894
PETER
T.
BOAG
SMITH, J. N. M., AND A. A. DHONDT. 1980. Experimental confirmation of heritable morphological variation in a natural population of song
sparrows. Evolution 34:1155-1158.
SMITH, J. N. M., AND R. ZACH. 1979. Heritability
of some morphological characters in a song sparrow population. Evolution 33:460-467.
SOKAL, R. R., AND F. J. ROHLF. 1969. Biometry.
netic-phenetic variation correlation. Nature 242:
191-193.
VANDENBURG, S. G., AND F. FALKNER. 1965.
Hereditary factors in human growth. Hum. Biol.
37:357-365.
VAN VLECK, L. D., AND C. R. HENDERSON. 1961.
Empirical sampling estimates of genetic correlations. Biometrics 17:359-371.
W. H. Freeman Co., San Francisco.
SOULE, M., S. Y. YANG, M. G. W. WEILER, AND
Corresponding Editor: S. J. Arnold
G. C. GORMAN. 1973. Island lizards: the ge-
This content downloaded from 132.174.254.72 on Mon, 06 Mar 2017 15:40:15 UTC
All use subject to http://about.jstor.org/terms