Inheritance of Size and Shape in a Population of Darwin's Finches, Geospiza conirostris

Inheritance of Size and Shape in a Population of Darwin's Finches, Geospiza conirostrisAuthor(s): P. R. GrantSource: Proceedings of the Royal Society of London. Series B, Biological Sciences, Vol. 220, No.1219 (Dec. 22, 1983), pp. 219-236Published by: The Royal SocietyStable URL: http://www.jstor.org/stable/35811 .

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Proc. R. Soc. Lond. B 220, 219-236 (1983) Printed in Great Britain

Inheritance of size and shape in a population of Darwin's finches, Geospiza conirostris

BY P. R. GRANT

Division of Biological Sciences, University of Michigan, Ann Arbor, Michigan 48109, U.S.A.

(Communicated by W. D. Hamilton F.R.S. - Received 25 April 1983)

Mass, wing length, tarsus length and four bill dimensions were measured on adult Large Cactus Ground Finches (Geospiza conirostris) and their offspring in a field study on Isla Genovesa, Galapagos. Heritabilities of these traits were determined by regressing family mean offspring values on midparent values. Principal components analysis was used to provide a multivariate characterization of size and shape, and component scores were used in heritability analysis.

Morphological traits were highly heritable. All heritabilities of univariate traits exceeded 0.65, and the arithmetic mean was 0.84. Principal component 1 provides a measure of overall body size; this has a high heritability (0.79). Principal component 2, a bill-pointedness shape factor, also has a high heritability (0.92). Indirect evidence suggests the possibility of a small influence of genotype-environment correlation on the heritability estimates for two traits, mass and bill length. The overall conclusion is that there is a strong potential for evolutionary change in morphology in this population. The population may have been subject to disruptive selection recently, followed by stabilizing selection.

Genetic correlations between measured traits were moderately large (mean 0.54) and all were positive. In several respects G. conirostris is intermediate between two other congeneric species, G. fortis and G. scandens. Heritabilities and genetic correlations appear to be higher in G. fortis and lower in G. scandens. These differences are associated with different feeding niches, different degrees of predictability of food resources and different types of selection pressures to which the species are subjected.

1. INTRODUCTION

The evolutionary dynamics of a population are governed by the amount and dispersion of genetic variation within the population, and the forces acting upon that variation. A highly unusual distribution ofphenotypic variation was discovered in 1978 in a population of Darwin's finches (Grant & Grant I979). On Isla Genovesa, Galapagos, males of the Large Cactus Ground Finch (Geospiza conirostris) sing one of two songs, either a slow A song or a fast B song. Beaks of the A males were found to be 6 % longer on average than beaks of the B males (figure 1), but not deeper or wider. In the dry season, when finch population sizes in general are likely to be limited by a diminishing food supply (Smith et al. 1978; Grant & Grant

[ 219]



220 P. R. Grant

1980; Schluter 1982), the two groups of males fed in different ways (Grant & Grant

I979). These observations on morphological and ecological subdivision gave rise to the speculation that the population had reached an early stage of speciation under a regime of disruptive selection.

For the proposed selection to have evolutionary consequences it is necessary that there be significant genetic variation underlying the phenotypic variation in beak

17-

16-

D 15- * _ o

14- o

13 I I I i o j 9 10 11 12 13 14

bill depth/mm FIGURE 1. Beak characteristics of two groups of Geospiza conirostris males in 1978, those singing

song A (i) and those singing song B (o). The two groups differ significantly (p < 0.002) in bill length but not in bill depth. From Grant & Grant (I979).

length. This paper presents the results of a field investigation, the primary purpose of which was to determine the inheritance of beak length and other morphological traits in the population. Ecological studies of the structure of this population have also been conducted (Grant & Grant i983), and their relevance to the results

presented in this paper is considered in the discussion. Several morphological traits including beak length are known to be highly

heritable in a congeneric species, the Medium Ground Finch Geospizafortis on Isla

Daphne Major (Boag & Grant 1978; Boag I983). High heritabilities in one

population are not necessarily a reliable guide as to what to expect in another

population of another species in another environment, for a variety of theoretical reasons (for example, see Feldman & Lewontin 1975). Furthermore, the sympatric Cactus Ground Finch species on Isla Daphne, G. scandens, displays generally low heritabilities (Boag 1983). Information to date on G. conirostris itself is no more than suggestive. Nestling measurements taken in 1978 were regressed on mid-parent values. The slopes of the regressions were high and significantly different from zero for some dimensions, for example beak depth, but lower and not significantly different from zero for others including the important one, bill length (Grant

981 a). It was therefore an open question as to whether observed phenotypic variation in beak length in this species is governed by detectable genetic variation. The question is addressed in this paper with analyses of data from offspring (of measured parents) that were captured and measured when fully grown.

A second purpose of the investigation was to estimate the phenotypic, genetic



Darwin's finches

and environmental correlation structure of G. conirostris, because directions and rates of evolution are determined by the correlation structure. The results are

compared in the discussion with similar estimates for G.fortis and G. scandens (Boag 1983), and from this comparison inferences are made about genetic processes occurring in the evolutionary diversification of Darwin's finches.

2. MATERIALS AND METHODS

2.1. Measurements

Adults were captured in mist nets, measured, individually colour-banded and released in each of the years 1978-1982. Nestlings were measured and banded when

eight days old in all years except 1979. Fifty-three nestlings were subsequently recaptured and measured at ages varying from 27 d to about 900 d.

Seven morphological variables were examined. Measurements were taken as follows: mass, with a Pesola spring balance; wing length, from carpal joint to the

tip of the longest primary; tarsus length, from tibiotarsal joint to a distal, identifiable, undivided scute; bill length, from anterior edge of nostril to tip of upper mandible; bill depth, in the vertical plane level with the anterior edge of the nares; bill width (U), at right angles to the bill depth measurement on the upper mandible; bill width (L), at the base of the lower mandible. Mass was measured to the nearest 0.1 g, wing length was measured to the nearest millimeter and the remaining dimensions were measured to the nearest 0.1 mm.

The majority of measurements were taken by the author. Others were taken by two assistants, T. C. Will and D. J. Anderson. Small corrections were applied to measurements taken by the assistants on the basis of differences between the measurements of 24 adults measured by T. C. Will and the author and 25 adults measured by D. J. Anderson and the author: differences in means between

investigators were in the range of 0-2.5 %. Seventeen adults were measured by the author twice, permitting calculation of repeatabilities, that is the percentage total variance from a one-way analysis of variance attributable to differences among birds (see Falconer 1981, p. 126). The individual that gave rise to the outlier in

figure 1 was not included. Since there were no systematic changes between successive measurements of the same bird, the first set of measurements was used in the analyses: there was little accuracy to be gained from averaging multiple measurements because less than half of the birds measured twice entered the

heritability analyses. 2.2. Analysis

Heritabilities were calculated from regression analysis. Offspring measurements were regressed on father, mother or midparent values. The heritability of a trait is the slope of the midparent regression, and twice the slopes of the single parent regressions. Since almost all families were represented by a single offspring I did not use a family-size weighting technique (Falconer 1963), unlike Boag (1983) in his analysis of G. fortis and G. scandens. Instead I averaged the offspring measurements in the five families represented by more than one offspring. Samples were not sufficient to standardize the data for both sex and year as Smith & Zach

221



(I979) did in their analysis of Song Sparrows, Melospiza melodia. Inspection of the data revealed no obvious heterogeneity between broods and years, and the sexes were apparently equally represented in the offspring: of 22 offspring of known sex, 12 were males and 10 were females. In all other respects the methods used here were the same as those used by Boag (1983), thus facilitating a congeneric comparison of results.

Principal components analysis was used to provide multivariate characterizations of size and shape. This analysis was restricted to 20 families of fathers, mothers and offspring with complete data. Four families had more than one offspring, but only the eldest offspring in each case was included for analysis, so that each family was represented by only one offspring measured at an age of at least ten weeks when growth had almost or entirely ceased (see next section). The cube root of mass was used to make it commensurate with the dimensions, upper bill width was deleted to avoid duplication with the highly correlated covariate lower bill width, the six remaining variables were lg-transformed and then principal components were extracted from covariance matrices generated from the combined sample of parents and offspring. Principal component scores of parents and offspring were used in heritability analysis to suggest the overall phenotypic qualities most strongly inherited. Phenotypic, genetic and environmental correlation analyses were performed with In-transformed data.

The heritabilities of morphological traits and the genetic and non-genetic correlations among traits were calculated by applying the standard techniques of quantitative genetics to measurements of these offspring and their known parents (Falconer 1981; see also Boag 1983).

2.3. Sources of variation

Potential distortions to the estimates of heritability can arise from incomplete growth of some offspring in a sample heterogenous with respect to age, low repeatability of measurements, unequal variances of parental traits and assortive mating with respect to those traits.

Boag (1983) found that adult mass, wing length and tarsus length are closely approached or reached before six weeks old, but that growth of bill dimensions reaches an asymptote in G. fortis at eight weeks after hatching, while bill length in G. scandens takes up to 12 weeks to approach an asymptote. Composite growth curves show that G. conirostris is intermediate (table 1, figure 2). Therefore in most of the subsequent analyses a restricted sample of offspring at least ten weeks old is used to minimize the effects of age. By ten weeks asymptotic size has been reached in all traits except bill length and depth, and for these two traits 99.8 % of asymptotic size has been reached. Descriptive statistics of these 28 offspring and their parents are given in table 2.

Mean offspring measurements are intermediate between mean male and mean female measurements, with two exceptions: mean mass and bill length are lower than means of both parents (table 2). This shows that even though asymptotic size has been reached by about day 70, further growth in these traits remains. A small amount of growth probably takes place at about one year old, perhaps at the time of the first full moult, as shown by the fact that the 17 offspring measured at ages

222 P. R. Grant



Darwin's finches 223

TABLE 1. PARAMETER ESTIMATES FOR THE LOGISTIC GROWTH MODEL FITTED TO

MEASUREMENTS OF SIX TRAITS OF G. CONIROSTRIS

A age

mass/g 24.13+0.28 46 0.3073+0.0126 wing length/mm 74.67+1.65 35 0.3492+0.0184 tarsus length/mm 22.64 +0.17 33 0.3785 +0.0101 bill length/mm 14.17+0.10 75 0.1417 +0.0062 bill depth/mm 10.30 +0.08 80 0.1245 +0.0066 bill width/mm 6.29+0.06 70 0.1643+0.0089

See also figure 2. A is the estimated asymptotic value for each trait, age is in days at which it is reached, r is the estimated characteristic growth rate. 95 % 'support plane' confidence intervals are given for the growth parameter estimates (after Dunham 1978).

30 , 16

2 0.- - ': -12 20-

. ;,

;-16 20 -

f*J /

,/ - / g8 S 10- / - /

/ _, .. _- 4 4 0 ' I I ' ' 0

V V V V 25 I I I . 12

20- 1 ~.~ 15- , . - /' -8

.

- 10 , v

5-

0o i I I 0 1 10 100 1000 1 10 100 1000

age/d FIGURE 2. Growth curves for four traits, plotted semi-logarithmically for scaling convenience:

see table I for parameters of the growth equations. Symbols: u daily means for nestling measurements, taken from Grant (I98Ia); * measurements of individual fledglings; v modal day of fledging; v modal day of departure from natal territory, taken from Grant & Grant (I980).

from 300-900 d had longer beaks than the 20 measured at ages 70-160 d. Mean bill length of the older group (14.78 mm) is also intermediate between parental means. Strictly, further growth renders the logistic model inapplicable to mass and bill length because the assumption that the parameters are time-invariant over the intervals covered by the measurememeasurements is not met. Nevertheless asymptotic sizes are estimated quite closely (compare tables 1 and 2).

Repeatability of adult measurements is generally high (table 2). Values are similar to those obtained by Boag (I983) over a shorter period, from a few days to three years. As in his study, repeatability was lowest for mass and highest for bill width. Repeatability, in the sense used here, reflects both real changes in



dimensions between measurement periods and the constancy of measurements (measurement error). Mass is well known to fluctuate diurnally and seasonally in relation to the physiological state of the bird. Similarly, wing feathers and beak tips become abraded seasonally, but are then replaced with longer feathers (wing) and regrown (beak tip). The other dimensions are not subject to these fluctuations, and their measurements are more repeatable. The high repeatabilities overall preclude a serious distortion of heritability estimates.

TABLE 2. MEASUREMENTS OF G. CONIROSTRIS PARENTS AND OFFSPRING MORE

THAN TEN WEEKS OLD

male female offspring repeatability

mass/g 25.92+ 1.96 24.54 +2.16 24.26+2.11 0.714 wing length/mm 78.28 ? 2.36 74.00 + 2.85 74.41 +2.47 0.865 tarsus length/mm 22.59+0.67 21.69+1.04 22.05+0.78 0.880 bill length/mm 14.83+0.83 14.56 +0.85 14.36 +0.94 0.781 bill depth/mm 11.03+0.82 10.01+ 1.03 10.42+0.68 0.940 bill width (U)/mm 6.71 +0.42 6.25+0.35 6.45+0.31 0.951 bill width (L)/mm 10.18+0.62 9.37+0.67 9.61+0.65 0.977 N 28 23 28 17

Only the eldest offspring from the five families represented by more than one offspring has been included in the calculations. Means with one standard deviation are shown. Repeatabilities are given for traits measured twice, one to four years apart, on 17 adults. N = sample size. U and L stand for upper and lower.

TABLE 3. CORRELATIONS BETWEEN MATES

correlation coefficient (r)

mass/g -0.354 wing length/mm 0.249 tarsus length/mm 0.010 bill length/mm -0.010 bill depth/mm 0.114 bill width (U)/mm -0.041 bill width (L)/mm -0.216

Sample size is 20; for this sample size, the correlation is significant (p < 0.05) when r = 0.444. U and L stand for upper and lower.

Variances of male and female parents are similar for each of the traits. Furthermore there is no evidence for assortive mating with respect to any of the traits (table 3; see also Grant & Grant 1980). Boag & Grant (1978) found significant positive correlations between mates of G. fortis on Isla Daphne Major for some

morphological traits in 1976, but in 1978 there were no such associations between mates (Boag 1983).

Estimates of heritability are distorted when genotypes are distributed non-

randomly among environments. This problem will be considered in the discussion.

224 P. R. Grant



Darwin's finches

3. RESULTS

3.1. Univariate analyses

Heritability estimates are given in table 4. Heritabilities calculated from the

midparent regressions are all high and significantly different from zero. A few exceed the theoretical maximum of 1.0 but not to a statistically significant extent. Their arithmetic mean is 0.84. Four of the regressions are shown in figure 3.

TABLE 4. HERITABILITIES AND ONE STANDARD ERROR CALCULATED USING ONLY

OFFSPRING AGED 70 D OR OLDER

mass/g

wing length/mm

tarsus length/mm

bill length/mm

bill depth/mm

bill width (U)/mm

bill width (L)/mm

p.c. 1

p.c. 2

p.c. 3

p.c. 4

father-offspring

0.54 + 0.38 27

1.03 +0.36** 28

0.95 + 0.43* 27

1.37 + 0.36*** 28

0.69 + 0.29* 28

0.67 + 0.26* 27

1.04 + 0.37** 27

0.95 + 0.49 26

1.48 +0.28** 26

0.76 + 0.43 26

1.73 +0.42** 26

mother-offspring

1.02 + 0.38* 22

0.67 +0.36 23

0.81 +0.28* 21

1.00+0.33** 23

0.92 +0.14*** 23

1.21 +0.20*** 23

0.76 + 0.28* 22

0.86_0.15*** 21

1.12 +0.43* 21

0.55+0.33 21

0.49 + 0.43 21

midparent-offspring 1.09+0.27***

21 0.69 +0.21**

23 0.78 +0.23**

20 1.08 +0.19**

23 0.69 +0.09***

23 0.81 +0.18***

22 0.77 +0.25**

21 0.79+0.15***

20 0.92 +0.17***

20 0.52 + 0.21*

20 0.93 + 0.30**

20

Sample sizes are given beneath the heritabilities. U and L refer to upper and lower, and p.c. is principal component. Statistical significance is indicated by * (p < 0.05), ** (p < 0.01) or *** (p < 0.001).

Inclusion of eight offspring (from different parents) measured when 27-68 d old, to increase the sample sizes, has little effect upon the heritability estimates. Not surprisingly they have the greatest effect upon mass and bill length, the two traits that change most with age during this period (figure 2). Inclusion of the offspring reduces the heritabilities of the two traits to 0.85 and 0.94 respectively, but the significance levels remain unaltered.

The single parent regressions are all statistically significant with the exception of paternal mass and maternal wing length. Mother-offspring heritabilities are not consistently larger than father-offspring heritabilities, therefore maternal effects are probably minimal. Inclusion of the small sample of 27-68 d old offspring in the total sample has minor effect on these heritability estimates.

Table 4 provides a comparison of heritabilities calculated from measurements

225



P. R. Grant

midparent mass/g 21 25 29

I I S

-0 ?*?

0

0

/ I

* I

I i e

0

/

I

* 0

I I

21 22 23

midparent tarsus length/mm

midparent bill length/mm 14 15 16

?/ ?

7 / * 0

/ 0S 0/ .

* -]

0/ I I

o 0

_ /* _

0 0 0

//

I0* I

0 0

S

15

14

-10 r

9

9 10

midparent bill width/mm

FIGURE 3. Regressions for four traits. The heritability is the slope. (see also table 3).

TABLE 5. COMPARISON OF HERITABILITIES CALCULATED BY THE OFFSPRING-

MIDPARENT REGRESSION TECHNIQUE APPLIED TO LN-TRANSFORMED MEASURE-

MENTS OF DIFFERENT BIRDS IN TWO AGE GROUPS

age of offspring d

mass/g wing length/mm tarsus length/mm bill length/mm bill depth/mm bill width (U)/mm N

11

1.32 + 0.59* -1.73 + 1.36

0.89+0.19** 0.89 + 0.57 1.03 +0.19*** 0.91 +0.19***

10

> 70

1.08+0.27** 0.72 +0.21** 0.79 +0.22** 1.09+0.19*** 0.71 +0.08*** 0.82+ 0.18***

23

Data for 11-day nestlings are taken from Grant (1981 a). Note the similarity of estimates for 11-day nestlings and for the independent offspring, except for the two traits with most additional

growth remaining at day 11, wing and bill length. Statistical significance is indicated by * (p < 0.05), ** (p < 0.01) and *** (p < 0.001). Other symbols as in table 3.

of offspring fully grown or almost so with those calculated from measurements of

day 11 nestlings. For this comparison all measurements were In-transformed before

analysis; transformation has only trivial effects upon heritability estimates for the older group of offspring (compare tables 4 and 5) but moderately large effects on some estimates for the nestlings (see Grant i 98 a). The results in table 5 show that the estimates of heritabilities of most traits remain unchanged after this stage of

226

-5

S

S 25 21

0 21

S

23

4-4

1 22

I, b= 21

o

S -

be

-

.0

bl0

b,

r_?

0

F- FLI



Darwin's finches

nestling development has been reached. Furthermore the two traits for which

significant heritabilities were not found in the nestling stage, wing length and bill

length, are shown to be significantly and highly heritable in the sample of fully grown birds.

3.2. Multivariate analyses The implication of the consistently high heritabilities for the seven traits is that

overall size, however measured, has a high heritability. This is borne out by the results of principal components analysis. The first principal component (p.c. 1) is

highly heritable, as shown by the result of offspring-midparent regression (table

TABLE 6. CORRELATIONS BETWEEN CHARACTERS AND PRINCIPAL COMPONENT

SCORES

p.c. 1 p.c. 2 p.c. 3 p.c. 4

mass/g 0.75 0.15 0.06 0.17 wing length/mm 0.62 -0.02 0.47 0.54 tarsus length/mm 0.67 0.08 0.27 0.20 bill length/mm 0.73 0.66 -0.17 -0.02 bill depth/mm 0.92 -0.13 0.28 -0.21 bill width (L)/mm 0.90 -0.28 -0.30 0.07 eigenvalues x 10-4 27.01*** 4.56*** 3.55** 1.74** % variance 68.75 11.59 9.04 4.42

Principal components were extracted from the covariance matrix of the In-transformed data. The sample size was 85 parents and offspring more than ten weeks old, all with complete measurements. Significance of each eigenvalue was assessed by a X2 test for sphericity; there are insufficient degrees of freedom to test beyond p.c. 4. Statistical significance is indicated by ** (p < 0.01) and *** (p < 0.01).

4). Traditionally p.c. 1 has been interpreted as a composite size factor because all variables contribute to it strongly and positively (for example see Gould & Johnston 1972). This is certainly the case in the present instance in the combined sample (table 6), as well as in the male sample, female sample and offspring sample treated separately. Thus size is a highly heritable trait in G. conirostris.

The heritability of additional, composite, shape variables can be assessed with other principal components. Offspring-midparent regressions show that p.c. 2, 3 and 4 scores are heritable (table 4). Table 6 helps to interpret these results in terms of the original variables. It can be seen that p.c. 2 is dominated by bill length. In addition, by the signs of the coefficients it can be seen that the contribution of bill length to p.c. 2 varies inversely with the contributions of bill depth and width. Therefore, p.c. 2 may be described as a heritable bill pointedness factor.

Principal components 3 and 4 are best interpreted as factors representing bill proportions in relation to the size of other traits. The components explain only 13.5% of total variation in the combined sample (table 6). With such a small amount of variation explained it is noteworthy that any detectable heritable variation exists.

These results for G. conirostris are similar to those obtained for G. fortis by Boag

227



P. R. Grant

( 983). The amount of variation explained by the first four components is almost identical in the two cases (see Boag 1983), and in each case there are statistically detectable heritabilities for all four components. In both cases p.c. 1 is best

interpreted as a size factor. In both cases p.c. 2 is best interpreted as a bill

pointedness factor. G. scandens differs from both in displaying significant heritabilities for shape factors only (p.c. 2 and 4), and not size (p.c. 1), although like the other two species the most important shape factor (p.c. 2) can be

interpreted as a measure of bill pointedness.

3.3. Correlation structure

In the combined sample of males, females and offspring, all phenotypic traits are strongly correlated with each other, as well as with p.c. 1 (tables 6 and 7). Males, females and offspring have similar phenotypic correlation structures.

The observed phenotypic correlations are governed by genetic and environmental causes. In principle these causes can be separately estimated by calculating genetic and environmental correlations, that correspond to the partitioning of the covariance between traits into the additive genetic component and all of the rest (Falconer 198 , p. 282). The rest includes the non-additive genetic component, but for metric traits like these such effects are often assumed to be small. Thus the genetic correlations express the degree to which individual genes or genes in linkage disequilibrium affect two or more characters. If we ignore non-additive genetic effects, the environmental correlations express the degree to which two characters respond similarly to variations in environmental conditions.

When characters have high heritabilities it is to be expected that phenotypic correlations are mainly determined by the genetic correlations. This expectation is realized here (table 7). Often genetic correlations are higher than phenotypic correlations among morphological traits (for example see Atchley et al. 198I; Cheverud 1982). Here the genetic correlations are generally large and close to the values for the phenotypic correlations. Like the phenotypic correlations, they are all positive. The arithmetic mean of the 21 genetic correlations among the seven univariate traits is 0.58.

Genetic correlations between bill length and the other dimensions are conspic- uously low: their arithmetic mean is only 0.39, four of the six are less than 0.45 and three are among the lowest four in the whole set. Thus genetically, as well as

phenotypically, bill length tends to vary independently of the other measured traits.

With such high heritabilities and moderate genetic correlations, it follows that non-additive genetic and environmental causes of the phenotypic correlations will be relatively small. This is a consequence of the partitioning of the covariance between traits, discussed above. Their magnitude will vary in proportion to the difference between corresponding phenotypic and genetic correlations weighted by the heritabilities. Table 7 shows that the estimates of environmental correlations between traits vary greatly and are often large. Because they are not properly bounded by -1.0 and +1.0, little significance can be attached to the exact

magnitude of individual correlations. Nevertheless, in the aggregate there is an inverse relationship between the strength of the genetic and environmental

228



phenotypic correlations (rp) mass/g wing/mm tarsus bill length/mm bill depth/mm bill width (U)/mm bill width (L)/mm p.c. 1 p.c. 2

genetic correlations (rG) mass/g wing/mm tarsus/mm bill length/mm bill depth/mm bill width (U)/mm bill width (L)/mm p.c. 1 p.c. 2

TABLE 7. GENETIC AND NON-GENETIC CORRELATIONS AMONG TRAITS

bill bill bill mass wing tarsus length depth width (U)

g mm m m mm mm mm

environmental correlations (rE)

0.129 -1.156 -0.407 1.004 0.542 - 1.128 0.836 0.736 0.499 0.465 - -0.771 0.892 0.618 0.365 0.461 - 2.311 0.670 0.602 0.605 0.547 0.685 0.484 0.596 0.548 0.812 0.631 0.458 0.516 0.527 0.779 0.754 0.623 0.667 0.729 0.925 0.153 -0.018 0.085 0.657 -0.131

-0.301 0.127 0.744 2.687 0.622

0.678 0.803

-0.006

standard errors for rG

0.123 0.092 0.093 0.078 0.593 0.172 0.148 0.091 0.706 0.253 - 0.097 0.093 0.601 0.262 0.612 - 0.096 0.585 0.549 0.513 0.199 0.767 0.595 0.605 0.217 0.877 0.558 0.573 0.800 0.454 0.893 0.742 0.618 0.766 0.566 0.903 0.282 -0.098 0.212 0.804 -0.405

0.068 0.116 0.110 0.132 0.030

0.862 0.860

-0.326

bill width (L)

mm p.c. I p.c. 2

0.870 0.504 -1.616 0.076 0.650 -0.663

-0.671 0.294 -0.750 0.770 1.484 -5.972 0.426 1.009 -3.082

--0.174 0.567 -2.393 0.646 -2.956

0.905 - - -0.280 -

0.132 0.068 0.128 0.141 0.112 0.165 0.073 0.066 0.153 0.127 0.087 0.045 0.026 0.018 0.087 0.046 0.037 0.129

- 0.010 0.163 0.968 -

-0.155

Genetic and environmental correlations were calculated according to methods discussed by Falconer (I981): the original data were from 20

families each represented by one offspring more than 70 d old, and the heritabilities used in the calculations are the estimates from

offspring-midparent regressions listed in table 4. U and L stand for upper and lower respectively.



correlations (r = -0.69). Correspondingly phenotypic and genetic correlations are positively associated (0.53), whereas there is no systematic association between environmental and phenotypic correlations (0.15). Cheverud (I982) obtained similar results in a study of rhesus macaques (Macaca mulatta), but such relation- ships are not universal (for example see Hegmann & deFries 1970).

4. DISCUSSION

4.1. The magnitude of heritabilities

The overall conclusion from this study is that the morphological traits chosen for analysis are highly heritable. The few passerine bird species studied in a similar way also have high heritabilities (Boag & Grant 1978; Boag 1983; Dhondt 1982; Garnett 1981; Smith & Zach I979; Smith & Dhondt 1980; van Noordwijk et al. 1980), but the heritabilities of G. conirostris are, if anything, higher than those in the other species. Just how high they are is not certain. Some obvious sources of bias in the heritability estimates were not present in this study, as discussed in section 2.3, but there remain less tractable ones.

Heritability estimates will be distorted if selection has occurred on the offspring before the time at which samples of them are captured and measured. As a check on this possibility, I compared the nestling masses of the individuals subsequently recaptured with the nestling masses of their sibs that were not recaptured and, separately, with the masses of all nestlings not recaptured. I found no evidence of bias. For example, in the first comparison neither small or large individuals were

over-represented in the samples that were captured, either in the sample as a whole or in separate subsamples from large and small parents respectively.

Heritability estimates can be distorted if there is a correlation between

genotypes and environments (Falconer 1981). Where the influence of such correlations has been sought in other field studies of passerine birds, by techniques of experimental manipulation (Smith & Dhondt 1980; Dhondt 1982) or correlation

analysis (Boag & Grant 1978; Boag 1983; see also van Noordwijk et al. 1981), they have either not been detected or have been found but were small. In the present study, genotype-environment correlations may have had a small influence on some of the heritability estimates if, for example, genetically large parents had the best territories on which to raise their young.

Most growth of G. conirostris occurs in the nest (figure 2; see also Grant 1981 a). Most of the remaining growth occurs in the next 10-20 days (figure 2), and sometimes longer, while the fledglings remain on the natal territory (Grant & Grant

1980). Residual growth, particularly in body mass and bill length, is completed off the natal territory. In the years of this study, 1978-1982, fledging success was high and few instances of nestling runts were observed, so any genotype-environment effects are likely to have been small at this stage. If they arise they are likely to be larger in the fledgling stage, especially during the period on natal territory when the fledglings are learning to feed by themselves and are becoming independent of their parents. The incidence of mortality increases at this time. Since the growth of fledglings off-territory is conditioned by the stage of growth reached on-territory,

P. R. Grant 230



Darwin's finches

there is an interaction between possible influences of genotype-environment (territory) correlations and influences arising after those correlations have disap- peared when the fledglings have dispersed off-territory.

If the above reasoning is correct, it is to be expected that those traits that take the longest to reach final size, namely body mass and bill length (table 1, figure 2), will show the greatest distortion in the heritability estimates. This expectation appears to be realized, in that it is these two traits, and only these two, that yield estimates greater than 1.0 (table 4). I can find no evidence for an alternative explanation of these high slopes, that the offspring of the smallest and largest parents are heterogenous with respect to age at recapture and measurement. In contrast to mass and bill length, tarsus length is at approximately adult size in the nest at age 10 or 11 d (Grant 1981 a; also figure 2), and the slope of the regression on midparent value at this time is less than 1.0 and is similar to the slope calculated for much older fledglings (table 5). Tarsus, and bill dimensions other than length, have regression slopes of about 0.7 or 0.8, both as nestlings and as fledglings greater than ten weeks old. These values may be close to an unbiased estimate of the heritability of body mass and bill length.

4.2. The relevance of heritabilities to population subdivision

Whatever their exact magnitude, the high heritabilities demonstrate the potential for rapid evolutionary change in morphology. They also imply that the two song groups of males, which differed in bill length at the beginning of this study (1978), differed also genetically; for other indications of a genetic difference, see Grant & Grant (i979), (I983). It is still not known how or why the genetic difference arose, although disruptive selection is suspected (Grant & Grant 1979). The difference probably arose before or during the drought of 1977, which was well documented on another island (Boag & Grant 1981) but was also known to have occurred on Isla Genovesa (Grant & Grant 1980).

In each of the subsequent years rainfall has been plentiful and breeding has been extensive (Grant & Grant 1983). The population density has more than doubled, and its structure has changed. Male recruits fathered by males of the two song types have converged in bill lengths, with song A males having made the larger contribution to the convergence. The probable reasons for the convergence were identified (Grant & Grant I983) as, first, a tendency for (the large) song A males to mate in 1978 with females below average in size and, second, relaxation of the conditions that have been hypothesized to cause the initial difference in bill length between males. A model has been proposed to account for the changing population structure (Grant & Grant I983). It lays stress on alternating fusion and fission tendencies in a temporarily varying environment. The high heritabilities argue for these tendencies being genetic as well as phenotypic. This means that if fission tendencies persisted for several generations, a substantial amount of genetic differentiation could occur.

4.3. Interspecific comparisons and phylogenetic implications

During the adaptive radiation of Darwin's finches, certain morphological traits underwent more evolutionary change than others. The most evolutionarily labile

231



structure was the bill. Changes in bill size and proportions occurred during the process of speciation (Grant I98Ib). These changes may have affected the underlying correlation structures of morphology in some cases: certainly different regimes of stabilizing selection have different effects on correlation structure (Cheverud I982). Our best hope for understanding those past processes lies in

comparing closely related species, especially their respective morphological and genetic structures and their responses to contemporary regimes of natural selection (Boag & Grant 1981; Grant & Price i981; Price & Grant 1984).

The morphological and genetic structures of three species of Geospiza are now known in broad outline. These species are G. conirostris (present study), G. fortis and G. scandens (Boag I983). G. conirostris is larger than the other two in all dimensions, but in bill proportions it is intermediate between G. fortis (short, deep bill) and G. scandens (long, narrow bill). Correspondingly the feeding niche of G. conirostris is intermediate (Lack 1945, 1947; Grant & Grant 1982). The niche is most similar to the feeding niche of G. scandens, but G. conirostris feeds on some foods (Bursera seeds: Grant & Grant 1980) that G. fortis feeds on but which G. scandens does not, apparently because it is unable to crack the stones.

Lack (I945), (I947) argued, largely on the basis of plumage traits, that G. conirostris was relatively undifferentiated from the ancestral finches, whereas G. fortis and G. scandens were later derivatives (but see Yang & Patton 1981). If that were the case, then G. fortis and G. scandens would be the products of selection acting in opposite directions on a conirostris-like ancestral finch species. The data assembled in table 8 suggest that the genetic consequences have not been the same in the two lines of descent.

G. fortis is very similar to G. conirostris in total amount of phenotypic variation in each trait and in the proportion that can be attributed to the additive effects of genes (i.e. the heritability), whereas G. scandens differs from both in exhibiting lower levels of variation primarily due to the genetic component (Grant & Price

1981). In contrast, G. fortis is not especially similar to G. conirostris in correlation structure. Rather, G. fortis and G. scandens differ from G. conirostris in opposite ways. G. fortis has a tighter structure than G. conirostris: genetic correlations between traits are strong and all are positive. G. scandens has a looser structure than G. conirostris: most of the genetic correlations are small in G. scandens, and nine of the total of 15 are negative. These interspecific differences in genetic structure are paralleled by differences in phenotypic structure. On average phenotypic correlations are high in G. fortis, low in G. scandens and intermediate in G. conirostris. Thirteen of the 15 phenotypic correlations are larger in G. fortis than in G. conirostris, but 12 are larger in G. conirostris than in G. scandens.

Not all these differences between species are firmly established, and clearly better estimates of heritabilities and correlations are needed, especially for G. scandens. If it is assumed that morphological and genetic differences between the species have been correctly determined, they can be interpreted as consequences of the difference in the way in which species exploit the environment. The following interpretation integrates and extends the arguments of Boag (i 98, 1983) and Grant & Price (I981).

Each island environment varies substantially in the amount of annual rainfall

P. R. Grant 232



TABLE 8. MORPHOLOGICAL AND GENETIC CHARACTERISTICS OF THREE SPECIES OF GEOSPIZA

x mass/g wing/mm tarsus/mm bill length/mm bill depth/mm bill width/mm N

Xrp XrG XrE rp against rG rp against rE rE against rp

G. fortis c.v. h2

15.9 8.05 0.91 C 68.1 3.48 0.84 C 18.7 3.42 0.71 C 10.7 6.64 0.65 C 9.6 9.29 0.79 ( 8.7 6.60 0.90 C

44 78 39

0.66 0.84 0.46 (-0.13) 0.89

-0.12 0.13

G. conirostris G. scandens rp rG X c.v. h2 fp rG X c.v. h2 rp rG

).69 0.91 24.7 8.97 1.09 0.59 0.61 20.2 8.18 0.58 0.48 0.37 ).61 0.83 76.6 3.33 0.69 0.48 0.45 72.9 3.37 0.12 0.53 -0.09 ).55 0.73 22.1 3.94 0.78 0.51 0.58 20.6 3.64 0.92 0.33 0.45 ).68 0.88 14.7 5.99 1.08 0.50 0.43 14.5 4.75 0.32 0.40 -0.38 ).73 0.86 10.6 8.99 0.69 0.64 0.55 9.2 5.53 0.14 0.52 -0.07 ).71 0.83 9.8 7.87 0.77 0.56 0.66 8.6 4.78 0.34 0.49 -0.04

- - 45 45 23 1133 133 16 -

c0

0.55 0.54 0.81 (0.41) 0.53

-0.69 0.15

0.46 0.45 (0.04) 0.98 (0.67) 0.00 0.16 0.21

Values for G. fortis and G. scandens are from Boag (I981, I983); the rest are from tables 2, 4 and 7 in this paper and from Grant (98I a). Symbols: X mean; c.v. coefficient of variation; h2 heritability; rp average phenotypic correlation between one of the six traits and all of the rest; rG the same for genetic correlations; Xrp, XrG, XrE the average phenotypic, genetic and environmental correlations respectively for all traits. Numbers in parentheses are means calculated by taking into account the signs of the correlations; the means they stand next to are calculated without regard to the signs of the correlations. Correlations between correlation matrices are shown at the foot of the table.



234 P. . Grant

it receives and hence in the amount of primary and secondary production that occurs (Grant & Boag 1980). Responses to rainfall vary among plant species, and seed and fruit production is more consistent from year to year in some plant species than in others. A corollary is that food supply is more predictable for some finch

species than it is for others. Adaptive modification of bill structure to improve the

efficiency of exploitation of the predictable resources (e.g. Opuntia fruits by G.

scandens) has occurred, but the cost of such specialization has been the loss of an

ability to deal with some other foods (e.g. Bursera stones). The predominant selection regime on the specialist species is stabilizing in nature. Different selection

pressures are exerted on more generalist species, like G. fortis, that exploit unpredictable resources. Selection pressures fluctuate; at times they are stabilizing, at other times they are directional. Their net effect overall is stabilizing.

These facts suggest that differences between species in correlation structure are caused by differences in selection regimes. The differences in genetic structures feed back on the evolutionary process, because they set up different constraining influences on the course and rate of further evolution (compare with Lande 1979; Cheverud 1982). For example directional selection on a single trait such as bill

depth would produce strongly correlated responses in other traits in G. fortis, weakly correlated responses in G. scandens and intermediate ones in G. conirostris.

Geographical variation in G. fortis is consistent with the expected response to

simple directional selection on a trait. G. fortis populations differ among themselves almost entirely in average size of all traits. Furthermore the most closely related

species to G. fortis are scaled-up (G. magnirostris) or scaled-down (G. fuliginosa) versions of G. fortis, and there are only minor differences among all three species in patterns of dynamic and static allometry (Boag 1981; Grant I98Ia). As

expected, there are no other species like G. scandens but differing from it only in size. Interpopulation variation in this species has not been studied as well as it has in G. fortis, but there appears to be more variation in just bill shape than occurs in G. fortis (see Grant 1981 b). Little can be said about G. conirostris because there are essentially only two populations: they differ in size and shape (Lack 1945, 1947; Grant 198 b).

Notwithstanding the above reasoning and evidence, it as an open question as to whether genetic constraints have ever been important enough to affect the diversification of Darwin's finches. Given enough time, even the most contrained

species (G. fortis) could change under selection to the phenotype that makes

optimal use of resources on an island (Schluter & Grant 1984). The circumstance under which genetic constraints would be most detrimental is a situation of

interspecific competition, where initially neither species has the optimal phenotype. Depending upon the nature of the genetic constraints, the amount of genetic variation for selection to act on and the distance from the optimal phenotype, the species with the fastest rate of adaptive change would prevail by ultimately excluding the other.

The research was supported by grants from the National Research Council of Canada (A2920) and the National Science Foundation of the U.S.A. (DEB 77-23377 and DEB 79-21119). I thank the Charles Darwin Foundation, the Charles Darwin



Research Station staff, the Servicio Parque Nacional Galapagos and the Direccion General de Desarrollo Forestal, Quito, Ecuador, for permission to work on the

Galapagos and for other support. I am very grateful to B. R. Grant, K. T. Grant, N. Grant, D. J. Anderson and T. C. Will for field assistance, and to A. Dunham, T. D. Price and P. E. Smouse for help with the analysis. The manuscript benefited from critical comments given by P. T. Boag, T. D. Price and P. E. Smouse.

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Inheritance of Size and Shape in a Population of Darwin's Finches, Geospiza conirostris