The Influence of Seed Dispersal Mechanisms on the Genetic Structure of Tropical TreePopulationsAuthor(s): J. L. Hamrick, Darlyne A. Murawski, John D. NasonReviewed work(s):Source: Vegetatio, Vol. 107/108, Frugivory and Seed Dispersal: Ecological and EvolutionaryAspects (Jun., 1993), pp. 281-297Published by: SpringerStable URL: http://www.jstor.org/stable/20046315 .Accessed: 07/11/2011 12:58

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Vegetatio 107/108: 281-297, 1993.

T. H. Fleming and A. Estrada (eds). Frugivory and Seed Dispersal: Ecological and Evolutionary Aspects. 281

? 1993 Kluwer Academic Publishers. Printed in Belgium.

The influence of seed dispersal mechanisms on the genetic structure of

tropical tree populations

J. L. Hamrick, Darlyne A. Murawski1 & John D. Nason

Departments of Botany and Genetics, University of Georgia, Athens, G A 30602, USA; l Present address:

Biology Department, University of Massachusetts at Boston,Boston, MS 02125, USA

Keywords: Allozymes, Genetic diversity, Genetic relatedness, Population density, Seed shadows, Size

classes

Abstract

Seed dispersal mechanisms should have a direct impact on the genetic structure of populations. Spe cies whose seeds are dispersed near the maternal plant (e.g. gravity or wind dispersal) or species whose

seeds are deposited in clumps or patches should have more fine-scale genetic structure than species whose seeds are dispersed singly by mobile animals. Furthermore, due to the overlap of seed shadows,

species with high adult densities should have less genetic structure than species with lower densities.

Allozyme analyses of three tropical tree species belonging to the moist tropical forest of Barro Colorado

Island, Republic of Panama, were used to describe variation in the scale and intensity of genetic structure

within their populations. The genetic structure of seedlings and immature trees in the low-density,

wind-dispersed species (Platypodium elegans) was the coarsest and strongest whereas genetic structure

in a population of Swartzia simplex var. ochnacea (high density, bird-dispersed) was both the finest and

the weakest. The genetic structure ofAlseis blackiana, a high-density, wind-dispersed species was inter

mediate in both degree and scale. In P. elegans and A. blackiana, which had 'J' shaped size distributions, the significant genetic structure seen in the smaller and intermediate diameter classes disappeared in the

largest diameter class. The loss of genetic structure was not observed in S. simplex, a species with a more

even size distribution.

Nomenclature: follows Croat, T. B. 1978. Flora of Barro Colorado Island. Stanford University Press, Stanford. Ca. 943 pp.

Introduction

Seed dispersal patterns can shape the genetic

composition and structure of plant populations.

Species with limited seed dispersal are likely to

have considerable genetic heterogeneity among

patches of new seedlings while species with more

extensive seed dispersal should have less spatial

genetic structure (Fleming & Heithaus 1981; Howe 1989; 1990). Genetic structure is also af

fected by the interaction of seed dispersal with

other ecological and genetic processes. Seed dep osition patterns, pollen dispersal, adult densities,

microhabitat selection and several aspects of the

recruitment ecology of species could have signif icant effects on the patterning of genetic variation

within populations (Howe & Smallwood 1982; Howe etal 1985; Hamrick & Loveless 1986; Loveless 1991).

Sexually reproducing plants disperse genes in

282

two ways (Levin 1981). Male gametes are dis

persed twice; from the pollen parent to the ma

ternal parent via pollen and from the maternal

parent as part of the genetic complement of the

embryo. Maternal gametes, in contrast, move only once via seeds. The potentially greater variance in

the dispersal distance of pollen relative to seeds

may, in part, explain why knowledge of a species'

pollination system allows relatively accurate pre dictions concerning the distribution of genetic di

versity within and among plant populations

(Table 1 A). An equivalent understanding of seed

dispersal mechanisms provides less satisfactory

predictions of the distribution of genetic diversity

(Table IB). The range of among-population ge netic heterogeneity (FST) among seed dispersal

categories is not as large and the mean FST val ues are not consistent with the species' apparent

potential for seed dispersal. In particular, species with animal dispersed seeds have higher mean

levels of among population genetic heterogeneity than their potential for long-distance seed dis

Table 1. The distribution of allozyme variation at polymorphic loci within and among populations of plant species classified ac

cording to their breeding system and their seed dispersal mechanism. From Hamrick & Godt (1989).

Categories Na Mean no.

populations

Mean no.

loci

HT Hs

A. Breeding system

Selfing 78

Mixed-animal 60

Mixed-wind 11

Outcrossing-animal 124

Outcrossing-wind 134

B. Seed dispersal

Gravity 161

Gravity-attached 11

Attached 52

Explosive 23

Ingested 39

Wind 121

20.3

(3.8)c

8.9

(2.1)

10.0

(3.1)

10.7

(2.1)

10.7

(1.6)

10.1

(1.1)

29.2

(15.8)

20.8

(5.7)

12.4

(2.7)

17.6

(6.5)

8.7

(0.9)

16.2

(0.7)

14.4

(0.8)

12.5

(3.6)

17.7

(0.7)

16.7

(0.9)

16.9

(0.6)

18.6

(1.8)

16.5

(0.9)

18.6

(1.4)

13.2

(1.1)

16.6

(0.9)

NS

0.334abb

(0.016)

0.304b

(0.022)

0.378a

(0.057)

0.310b

(0.010)

0.293b

(0.011)

0.306b

(0.010)

0.211c

(0.038)

0.325b

(0.024)

0.302b

(0.021)

0.394a

(0.020)

0.292b

(0.012)

0.149c

(0.016)

0.221b

(0.017)

0.342a

(0.054)

0.243b

(0.010)

0.259b

(0.011)

0.207b

(0.011)

0.171b

(0.031)

0.236ab

(0.021)

0.217b

(0.023)

0.305a

(0.022)

0.241ab

(0.011)

0.510a

(0.035)

0.216b

(0.024)

0.100c

(0.022)

0.197b

(0.017)

0.099c

(0.012)

0.277a

(0.021)

0.124b

(0.031)

0.257ab

(0.032)

0.243ab

(0.048)

0.223ab

(0.033)

0.143ab

(0.020) a

N, number of taxa; HT, total genetic diversity; Hs, genetic diversity within populations; FST, proportion of the total diversity

among populations. Levels of significance: *** P< 0.001; NS, not significant.

b Means followed by the same letter in a column are not significantly different at the 5% probability level.

c Standard errors are in parentheses.

persal would indicate (Loveless & Hamrick 1984; Hamrick & Godt 1989; Hamrick etal 1991).

The magnitude of spatial genetic heterogeneity

resulting from seed dispersal depends on several

factors: (1) The proportion of seeds that immi

grate and contribute gametes to the next genera tion of an established population (i.e. gene flow) versus the proportion that colonize new habitats.

Slatkin (1977), and more recently Wade & Mc

Cauley (1988) and McCauley (1991), have shown that the colonization of vacant habitats is not

strictly analogous to gene flow among established

populations. Thus, if most seed movement is

among established populations there will be less

genetic structure than if the majority of the seeds

colonize newly available habitats; (2) The density of reproducing adults. If seeds from several adults

colonize an open habitat, genetic structure would

be less than if successful colonists had come from

one or a few adults. The effect of low adult den

sities should be especially apparent for wind

dispersed species. Maternal plant density un

doubtedly effects species with animal-dispersed seeds but may do so in less direct and predictable

ways; (3) The foraging and deposition behavior of

the seed dispersal agent. At one extreme are an

imals that forage within the canopy of a single individual and subsequently deposit several seeds

(at least half-sibs) in a site suitable for seedling recruitment. High genetic heterogeneity among recruitment sites will result, but may be tempered if several independent deposition events occur.

At the other extreme are seed dispersal agents that forage across several maternal individuals

and deposit seeds individually across the land

scape. This pattern of foraging and seed dispersal should produce less genetic structure among re

cruitment patches. In this paper these predictions are tested by

examining the fine-scale genetic structure of three

tropical tree species with different combinations

of seed dispersal mechanisms and population densities. The specific questions addressed in

clude: (1) Do neighboring individuals have higher genetic correlations (i.e. more al?eles in common) than individuals located farther apart? (2) Do

species with the same seed dispersal mechanisms

283

but with different adult densities maintain differ

ent levels of spatial genetic heterogeneity? (3) Do

species with similar densities but different seed

dispersal mechanisms have different levels of spa tial heterogeneity? (4) Does the spatial genetic

heterogeneity found in smaller size classes carry over into larger size

classe^?

Procedures

The study site is in the moist tropical forest of

Barro Colorado Island, Republic of Panama.

Barro Colorado Island (BCI) is the location of a

field station managed by the Smithsonian Trop ical Research Institute and of a 50 ha. Forest

Dynamics Plot (FDP) established by S. P. Hub bell and R. B. Foster. Every individual on the

FDP larger than 1.5 meters in height and 1 cm in

DBH has been identified and its location mapped

(Hubbell & Foster 1983; Hubbell & Foster 1990). Much of the research described below is located on the FDP because a 5 m x 5 m grid system al

lows efficient and accurate mapping of individu

als. The study site for Swartzia simplex var.

ochnacea was not on the FDP because the se

lected site had higher densities of this species. The forest of BCI and the FDP is the location

of a long-term study effort to describe the genetic structure (e.g. Hamrick & Loveless 1989) and the

breeding structure (e.g. Hamrick & Murawski

1990) of several tropical tree species. We are cur

rently studying the fine-scale genetic structure of

four species. These species were chosen because

they are relatively common on the FDP, their size

structure is indicative of active seedling recruit

ment, they maintain high levels of allozyme poly

morphism and they represent a variety of breed

ing systems, pollinator syndromes, life forms and

seed dispersal mechanisms.

Alseis blackiana Hemsl

Alseis blackiana (Rubiaceae) is a canopy tree with

bisexual flowers (Table 2). Little is known of its

breeding biology but its small, protogynous flow ers are probably pollinated by butterflies or small

284

Table 2. Characteristics of four tropical tree species studied for their fine-scale genetic structure.

Species Family Growth form Breeding system Pollinator Dispersal agent

Alseis blackiana

Brosimum alicastrum

Platypodium elegans Swartzia simplex var.

ochnacea

Rubiaceae

Moraceae

Fabaceae (Papil) Fabaceae (Caesal)

Canopy tree Bisexual

Canopy tree Dioecious

Canopy tree Bisexual

Understory tree Bisexual

Bees, Butterflies

Wind?, Insects?

Small bees

Large bees

Wind

Bats, Arboreal mammals

Wind Birds

bees. Alseis blackiana flowers in April or May and

its slender wind-dispersed seeds are released from

January to March during the dry season. Aug

spurger (1986) estimated that the mean seed dis

persal distance was 94 m with a wind speed of

1.75 m per second. Alseis blackiana is a common

canopy tree on the FDP with more than 230 in

dividuals greater than 32 cm DBH (Table 3). It also has a large number of smaller individuals

distributed throughout the FDP.

A one-hectare study site was established on the

FDP from which the basal diameter and map coordinates of approximately 1000 individuals of

all size classes were obtained. Adult individuals

(> 15 cm in diameter) were also sampled from a

20 m border surrounding the core study area

(Fig. 1 A). Leaf material was collected from each

individual, freeze-dried on BCI and returned to

the University of Georgia for electrophoretic

analysis. Every individual was genotyped for 31

polymorphic loci.

Brosimum alicastrum (Pitt) C. C. Berg

Brosimum alicastrum (Moraceae) is a dioecious,

insect-pollinated canopy tree (Table 2). It may

flower from November to May but the majority of

the flowering occurs from January to March.

Fruits mature from May to October and are eaten

by a variety of arboreal mammals. Monkeys have

been observed to eat the outer layers of the fruit

and to drop the seeds, often leaving a large ac

cumulation of seeds under the crown of the ma

ternal tree. Bats are thought to play a principal role in long-distance seed dispersal. Brosimum al

icastrum occurs at moderate densities on the FDP

(Table 3). It is somewhat unusual in that it does

not show a strong 'J' shaped age distribution in

the sapling stages (Table 3). Rather, individuals

in the 1, 2, and 4 cm diameter classes occur at

nearly equal densities.

Since Brosimum has relatively few individuals

on the FDP we have begun to genotype all tagged individuals. Unfortunately, this work is not yet

complete. We have systematically searched

60 m x 60 m areas around six known female trees

to determine seedling densities. The location and

size of each seedling was recorded. In order to

compare levels of seedling recruitment due to lo

calized seed dispersal with recruitment due to

long-distance seed dispersal, four 40 m x 40 m

plots, established at least 60 m from known fe

male trees, were similarly searched for seedlings.

Table 3. Size distribution of four tropical tree species located on the Forest Dynamics Plot on Barro Colorado Island. Data are

based on the 1985 census (Foster & Hubbell, unpubl. data).

Species

Alseis blackiana

Brosium alicastrum

Platypodium elegans

Swartzia simplex var. ochnacea

Diameter class (cm)

1 2 4

4137 2000 894 193 208 257 30 41 24

905 1000 688

8 16 32

451 335 212 137 45 32 26 5 12

174 20 0

Total

64 128

26 0 8055 25 1 898 17 2 157 0 0 2787

285

A) Alseis blackiana + < 15cm diameter O s: 15cm diameter

B) Platypodium elegans

C) Swartzia simplex var. ochnacea -*?o-s-o

Fzg. 7. The sampling areas used to study fine-scale genetic structure in three tropical tree species. A.Aleis blackania. The Aleis

study plot consisted of a one hectare study site surrounded by a 20 m border. B. Platypodium elegans. The FDP is shown with

the location of the 16 seedling shadow plots. C. Swartzia simplex var. ochnacea. The WH2 site is shown with the nested seed

ling plot. Seedlings and tagged plants are plotted.

Platypodium elegans J. Vogel

Platypodium elegans (Fabaceae) is a canopy tree

with perfect flowers that are pollinated by small

bees (Table 2). The large (mean fruit wt. = 2 g; fruit length

= 10 cm) one-seeded samaras are dis

persed up to 100 m by the prevailing north-east

winds during the dry season (Augspurger 1983).

286

Mean dispersal distances of 34 m were estimated

at wind speeds of 1.75 m per second (Augspurger

1986). Flowering is synchronous and may occur

twice a year, with many more seeds being pro duced in some years than in others (Augspurger

1983; Augspurger & Kelly 1984). Flowering gen erally occurs from April to June and fruits are

dispersed the following February to April. A large tree is capable of producing 4000-5000 seeds

during each flowering period. When seed produc tion is high, compact seed shadows are formed

downwind from the seed parent (Augspurger

1983). Every tagged Platypodium individual (> 1.0 cm

DBH) on the FDP was collected and genotyped for 24 polymorphic loci as part of the original

genetic survey of this species (Hamrick & Love

less 1989). To better analyze fine-scale genetic

structure, we established a 50 m x 100 m plot around each of 16 reproducing adults on the FDP

(Fig. IB). These plots extended 25 m upwind and

75 m downwind from each maternal individual.

Seedlings found within these plots were tagged,

mapped, and analyzed for 20 polymorphic loci.

Three 40 m x 40 m plots located at least 60 m

away from mature trees were also searched to

determine background levels of seedling recruit

ment outside of seed shadows associated with

maternal trees.

Swartzia simplex var. Ochnacea (A. DC) Cowan

Swartzia simplex var. ochnacea is an understory tree or shrub. It is bisexual and self-compatible

(Harcombe & Riggins 1968; Wyatt 1981) with

large showy lemon-colored flowers that are pol linated by large bees (Table 2). Swartzia flowers

in May or June and its fruits mature in Decem

ber or January. There are typically two to four

seeds per fruit and the seeds are bird dispersed.

Flowering and fruiting is highly irregular and un

predictable. Swartzia is a common element in the

understory of the FDP with nearly 3000 individ

uals above 1 cm in DBH (Table 3). Large indi

viduals are rare but individuals 4cm in DBH or

larger may flower and produce fruit.

The study site (WH2) was approximately 180 m x 70 m and was located in second-growth forest where Swartzia occurred at high densities

(Fig. 1C). In site WH2 every Swartzia individual

taller than 1.5 m was tagged, mapped, its basal

diameter measured, and a leaf was collected

for electrophoretic analysis. In a centrally located

area of about 110 m x 50 m (exact shape subject to dense treefalls) every plant below 1.5 m

was identified, tagged, measured, and collected.

Each individual was analyzed for 19 polymorphic loci.

Data analysis

Since the four species had been previously stud

ied, measures of genetic diversity among collec

tion sites separated by 100-200 meters on the

FDP were available (Hamrick & Loveless 1989). On the sites established to study fine-scale genetic

structure, individuals representing different diam

eter classes were divided into subplots and, where

sample sizes allowed, standard measures of ge netic structure were calculated. These included

Wright's (1951) FST and FIS values. The FST value measures the excess of homozygotes rela

tive to Hardy-Weinberg expectations in the pop ulation which are caused by al?ele frequency dif

ferences among population subdivisions (i.e. the

Wahlund effect). Thus, FST measures the level of

genetic heterogeneity among population subdivi

sions. The FIS value is the deviation from Hardy

Weinberg expectations within each population subdivision averaged over all subdivisions. A

positive FIS value indicates an excess of homozy

gotes within the subdivisions under consideration.

Statistical significance of FST values were exam

ined by chi-square test: %2 = 2N FST (a

- 1) with

df = (a

- 1) (n

- 1), where N is the total number of

individuals in the population subdivision, a is the

number of al?eles per locus, and n is the number

of population subdivisions (Workman and

Niswander 1970). The statistical significance of

FIS was also examined by chi-square test: y2 =

FIS

2N(a -

1) with df = (a -

1) (Li & Horowitz 1953). The FST and the FIS values were compared among

different diameter classes within species and were

also compared among species. Individuals within different diameter classes of

each species were compared to determine if near

neighbors have more al?eles in common than ran

domly chosen individuals. Three diameter classes

were chosen for the three species with genetic data (Alseis, 0-2 cm, 2-8 cm and > 8 cm; Platy

podium, 0-2 cm, 2-15 cm and > 15 cm; Swartzia, 0-2 cm 2-4 cm, and >4 cm.) For each diame

ter class the mean number of al?eles in common

per locus (NAC) between near-neighbors sur

rounding up to 100 different randomly chosen

focal individuals was calculated by modifying the

procedure developed by Surles etal. (1990). Where sample sizes were adequate this analysis was conducted for neighbor groups ranging from

two to 60 individuals. A grand mean and variance

for each near-neighbor group size was calculated

across the 100 focal individuals. The mean NAC

for a second set of individuals was calculated by

randomly sampling from 2 to 60 individuals of the

same diameter class for comparison. This proce dure was replicated 100 times for each group size

and mean NAC values were calculated. The NAC

values generated by the random comparisons were compared to the near-neighbor NAC values.

Ratios of the near-neighbor NAC value to the

random NAC value were calculated for each di

ameter class. These ratios were necessary for in

terspecific comparisons since species with more

genetic diversity will have lower NAC values.

Results

Alseis blackiana

A total of 999 individuals were sampled from the

one hectare study site on the FDP. The 0-2 cm

diameter class accounted for 794 individuals (0-1 cm = 517 individuals, 1-2 cm = 277 individuals)

while the 2-8 cm and > 8 cm diameter classes

had 168 and 37 individuals, respectively. Ten

adults were also sampled from a 20 meter border

surrounding the study plot. Distinct clumps of

individuals in the smallest diameter class were

287

found in a central location on the plot with a

sparse canopy and were not close to any adults.

Smaller clusters of individuals in the 0-2 cm and

2-8 cm diameter classes occurred on other parts of the study site (Fig. 1 A).

Measures of genetic diversity were calculated

at various spatial scales on the FDP and on the

one hectare study site. The four sample sites on

the FDP consisted of individuals greater than 1

cm DBH and were separated by approximately 200 m (Hamrick & Loveless 1989). The FST value

found among these four sites was 0.034 (Table 4),

indicating that moderate but significant heteroge

neity (x3 =

14.28;P< 0.001) in al?ele frequencies occurs at this spatial scale (Table 4). The mean

FIS value within each sample site (Table 5) was

0.104 (xi =

2.34; P<0.25). Since these sample sites included all diameter classes greater than

1 cm and covered rather large areas, the FIS value

includes, in addition to inbreeding, a Wahlund

effect among diameter classes and among spatial subdivisions within each sample site.

On the one hectare study site, different subdi

vision sizes were used for the three diameter

classes to insure that the FST and FIS values were

not affected by small sample sizes. A minimum of

15 individuals were required for a subdivision to

be included for analysis. Individuals in the 0-2

cm diameter class were assigned to 20 m x 20 m

subdivisions of the one-hectare study site to max

imize the number of subdivisions included in the

Table 4. Levels of genetic diversity among population subdi

visions (FST) of various spatial scales. The FST values on the

FDP represent collection sites separated by approximately 100 m (from Hamrick & Loveless 1989). The study sites were

subdivided at different spatial scales for the different diame

ter classes (I, II, III). See the text for the actual spatial scales

and diameter classes used for each species.

Species FDP Study site

Alseis blackiana 0.034

Brosium alicastrum 0.050

Platypodium elegans 0.051

Swartzia simplex 0.037

1 fST among seedling shadows.

I II III

0.041 0.027 0.015

0.091l

0.021 0.019 0.031

288

Table 5. Deviations from Hardy-Weinberg expectations

within population subdivisions (FIS) of various spatial scales.

The FIS values from the FDP are for collection sites separated

by approximately 100 m. The study sites were subdivided at

different spatial scales for the different diameter classes (I, II,

III). See text for the actual spatial scales and diameter classes

used for each species.

Species FDP Study site

I II III

Alseis blackiana 0.104 0.048 0.054 -0.014

Brosium alicastrum 0.120 - - -

Platypodium elegans 0.092 0.012l

Swartzia simplex 0.161 0.103 0.010 0.043

1 FIS within seedling shadows.

analyses. The FST value among the 14 subdivi

sions containing a minimum of 15 individuals was

0.041 indicating that highly significant heteroge

neity (#13 =

57.4, P< 0.001) in al?ele frequencies occurred among these arbitrarily defined subdi

visions. The FIS value over all loci was 0.048

(x\ =

1.61; P<0.25). To obtain adequate sample sizes for the 2-8cm diameter class, the one hect

are plot was divided into four 50 m x 50 m sub

divisions. The FST value among these subdivi

sions was 0.027 (xl =

4.07; P<0.05) and the FIS value over all loci was 0.054 (x?

= 0.49; P < 0.50).

The study site was divided into two equal subdi

visions for the analysis of the largest diameter

class. The FST value among these two sites was

0.015 (x?= 1.35; P<0.25) and FIS averaged across all loci was 0.014 (x\

= 0.009; P<0.99).

We also calculated FST among the three size

classes. The FST value was low (0.004) but was

significant (%^ =

7.26; P<0.05) because of the

large sample sizes involved. The mean FIS value

within each diameter class averaged across all

loci was 0.083 (/? = 6.94; P<0.010). The signif

icance of the FIS values indicates that there is a

significant h?t?rozygote deficiency within the di

ameter classes. However, since each diameter

class covered the one-hectare plot, the FIS values

include a significant spatial Wahlund effect. The

FIS value calculated for the spatial subdivisions

of each age class is largely free of this confound

ing effect and is more representative of the true

inbreeding coefficient.

In the 0-2 cm diameter class the number of

al?eles in common (NAC) among nearest neigh bors (1.399) was significantly higher (P<0.05) than the value for randomly chosen individuals

(Fig. 2A). The NAC values drop sharply as group size increases from 4 to 20 individuals. In near

neighbor groups of 20 to 60 individuals, NAC

values are nearly equal. Additional examination

indicated that the near-neighbor NAC value con

verges with the random NAC value at a group size of approximately 240 individuals. The ratio

of the near-neighbor NAC value to the random

NAC value for group size 2 was 1.032 and de

creased to 1.020 at group size 10 and to 1.018 at

group size 60 (Table 6). In the 0-2 cm diameter

class the mean distance of neighbors from the

focal individual was approximately lm for group size 2, increased steeply to approximately 5 m for

group size 20 and then increased more slowly to

7.6 m for group size 60 (Fig. 2A). The NAC value for near-neighbor individuals

in the 2-8 cm diameter class was 1.400 for a

group size two, and decreased sharply to 1.358

for group size 20 (Fig. 2B). For group size 60 the

NAC value was 1.338. The random NAC values

across all group sizes in this diameter class (1.335) were somewhat lower than that for the 0-2 cm

class. By group size 60 the near-neighbor NAC

Table 6. The ratio of near-neighbor NAC values to random

NAC values for different diameter classes and group sizes.

Species Diameter Group size

class -

(cm) 2 10 20 60

Alseis blackiana 0-2 1.032 1.040 1.020 1.019 2-8 1.040 1.034 1.025 1.002

>8 1.018 0.992 0.994 0.998

Platypodium elegans 0-2 1.071 1.042 1.031 1.001

2-15 1.064 1.036 1.017 1.000

>15 1.016 0.991 1.001 -

seedlings 1.049 1.079 1.060 1.062

Swartzia simplex 0-2 1.026 1.015 1.003 0.998

2-4 1.031 1.006 1.004 1.003

>4 1.037 1.013 1.011 1.010

289

A) 0-2cm diameter

1.46

20 30 40

Group size

B) 2-8cm diameter

1.46-1 Mean distance

Neighbor

Random

20 30 40

Group size

C) >8cm diameter 1.46

Mean NAC

1.384

1.364

1.344

1.32

1.30

Mean distance

Neighbor

Random

Mean distance

(m)

10 15 20

Group size 25 30

D) Mean NAC by distance 1.46

1.344

1.32

1.30

0-2cm diameter

2-8cm diameter

>8cm diameter

10 20 30 40 Mean distance (m)

50 60

Fig. 2. The relationship of near-neighbor and random NAC values for different group sizes or spatial separation of Alseis blackiana

individuals belonging to three diameter classes. A. 0-2 cm. B. 2-8 cm. C. >8 cm. D. The NAC values for the three diameter

classes versus distance among individuals being compared. Vertical bars represent ? one standard error.

had nearly converged with the random NAC

value. The ratio between the near-neighbor NAC

and the random NAC was 1.040 for group size 2, 1.025 at group size 20, and 1.002 at group size 60.

The mean distance separating an individual at the

center of a group from its near-neighbors was

about 3 m for group size 2, 10 m for group size 20

and nearly 21 m for group size 60 (Fig. 2B). For the largest diameter class (> 8 cm) groups

of more than 40 individuals could not be exam

ined because of the limited number of individuals.

The near-neighbor and random NAC values for

this diameter class were consistently higher than

values for the same group size in the smaller di

ameter classes (Fig. 2C). Nearest neighbors had

NAC values of 1.436 which decreased to approx

imately 1.386 at group size 20 and 1.393 at group

size 40. The NAC value dropped sharply from

group size 2 to group size 10 and then leveled off

at values somewhat below the random values.

The ratio between random and neighbor NAC

values was 1.018 for group size 2 and decreased

to 0.994 for group size 20 and to 0.998 for group size 40. The mean distance separating a central

individual from its neighbors was 10 m for the

nearest-neighbor comparisons and increased to

43 m when 30 individuals were compared

(Fig. 2C). NAC values were compared among the three

diameter classes as a function of the mean dis

tance separating individuals in a near-neighbor

group from its central individual (Fig. 2D). The

NAC values for the 0-2 cm and the 2-8 cm di

ameter classes decreased from approximately

290

1.417 and 1.400 to 1.364 and 1.338, respectively, as distance among neighbors increased (i.e. in

creasing group sizes). The curves for the two

smaller diameter classes were nearly identical. Al

though mean distances were much larger for the

largest diameter class and the NAC values were

also higher, the shape of the curve was similar to

that for the smaller diameter classes until approx

imately 20 m. Beyond 20 m there was no rela

tionship between NAC and mean distance among individuals.

Brosimum alicastrum

The only data on genetic differentiation presently available for Brosimum comes from the original

genetic surveys on the FDP by Hamrick & Love

less (1989). The level of genetic differentiation

(FST) among the four sample sites on the FDP

was 0.050 (xl =

28.80; P< 0.001). The mean FIS value across all loci was 0.120 (Xi= 4.15;

P<0.05). This FIS value includes a Wahlund ef

fect due to spatial and temporal genetic hetero

geneity. In order to compare recruitment due to local

ized versus long distance seed dispersal, the den

sity of seedlings in 60 m x 60 m plots centered on

six female individuals were compared to four

40 m x 40 m plots established 60 m away from

known females. The density of seedlings around

the maternal trees ranged from 0.0 to 1.83 seed

lings per 100 m2 with a mean of 0.99 (sd =

0.30)

per 100 m2. The range for the four 40 m x 40 m

plots was 0.06 to 1.00 individuals per 100 m2 with

a mean of 0.47 (sd =

0.23) individuals per 100 m2.

The mean seedling densities of maternal and

isolated plots are not significantly different due

to high among plot heterogeneity in seedling numbers.

Platypodium elegans

Seed shadows of 16 mature trees averaged 1.36

(sd =

0.61) seedlings per 100 m2. There was ex

tensive heterogeneity among adult trees with no

seedlings found associated with one adult, while

9.2 seedlings per 100 m2 were found around the

adult with the highest seedling density. No Platy

podium seedlings were found in three 40 m x 40 m

plots established in areas 60 m from adult trees.

Genetic structure in Platypodium was measured

at two spatial scales. First, genetic relationships between established individuals from throughout the FDP were compared. We also compared the

genetic relationships of seedlings within and

among the 50 m x 100 m plots centered around

16 adults. The level of genetic diversity among the

three collection sites located on the FDP (FST) was 0.051 (xl= 18.87, P<0.001) (Table4). The mean FIS value across all loci was 0.092 (x\

=

1.60; P<0.25) (Table 5). Comparisons of genetic

heterogeneity among the six seedling shadows

with more than 15 seedlings produced a FST value

of 0.091 (x25= 174.72; P< 0.001). The mean FIS value within the seed shadow plots was 0.012

(Z? = 0.14; P< 0.750). In the 0-2 cm diameter class located through

out the FDP the number of al?eles in common

among near-neighbors (1.530) was higher than

when random individuals were compared (1.426)

(Fig. 3A). NAC values decreased as group sizes

increased to six individuals. Beyond group size 10

there was a gradual convergence of the neighbor values to the corresponding random values. The

NAC ratio was 1.071 for group size 2, 1.031 at

group size 20 and 1.001 at group size 60 (Ta ble 6). The mean distance of neighbors from a

central individual in the 0-2 cm diameter class

was approximately 25 m for group size 2, increased to approximately 75 m for group size 10

and then increased to 275 m for group size 60

(Fig. 3A). The NAC value for near-neighbors in the 2-15

cm diameter class was 1.505 for group size 2 and

decreased to 1.415 for group size 20 (Fig. 3B). At

group size 60 the NAC had dropped to 1.395, and had converged with the random comparisons. Random comparisons within this diameter class

were equal to the random values for the 0-2 cm

diameter class. The ratio between the near

neighbor NAC and the random NAC was 1.067

for group size 2 but only 1.017 at group size 20

(Table 6). The mean distance of neighbors from

291

A) 0-2cm diameter 1.55

1.50

1.45

Mean NAC

1.40

1.35

1.30 20 30 40

Group size

B) 2-15cm diameter 1.55

1.50

1.45

1.40

1.35H

1.30

Mean distance

-,-.-1-1-1- -1-.-,-r 10 20 30 40 50 60

Group size

C) >15cm diameter 1.55-H

1.50

1.45 Mean NAC

1.40

1.35

1.30

- Mean distance

10 15 20

Group size

D) Mean NAC by distance

1.55

1.50

1.45 H

1.40

1.35

1.30

- 0-2cm diameter - 2-15cm diameter - >15cm diameter

0 50 100 150 200 250 300 350 400 Mean distance (m)

E) Seedlings in seed shadows

1.55

1.50

1.45 Mean NAC

1.40H

1.35

1.30

Mean distance

~8 Mean distance

6 (m)

20 30 40

Group size

Fig. 3. The relationship of near-neighbor and random NAC values for different group sizes or spatial separation of Platypodium

elegans individuals belonging to four diameter classes. A. 0-2 cm B. 2-15 cm C. > 15 cm D. The NAC values for the three di

ameter classes versus distance among individuals being compared. E. The NAC values for seedlings belonging to defined maternal

seed shadows. Vertical bars represent + one standard error.

a central individual was about 30 m for group size

2, 110 m for group sizes of 10 and 375 m for

group sizes of 60 (Fig. 3B).

There were fewer group sizes available for the

largest diameter class because of the limited num

ber of individuals. Near-neighbor NAC values for

292

this diameter class were consistently lower than

values for the same group sizes in the smaller size

classes (Fig. 3C). Nearest neighbors had NAC

values of 1.430 which changed to approximately 1.424 for group size 10. The ratio between ran

dom and near-neighbor NAC values was 1.016

for group size two and changed to 1.001 at group size 20. The mean distance separating individu

als from a central individual was 75 m for the

nearest-neighbor comparisons and increased to

340 m at group size 30.

The NAC values of the 0-2 cm and the 2-15

cm diameter classes were similar to each other in

having a close association with distance; as dis

tance among neighbors increased (i.e. increasing

group sizes) NAC values decreased from 1.525 to

approximately 1.400 (Fig. 3D). In contrast, for

the largest diameter class there was little relation

ship between NAC and distance.

NAC values were also calculated between

individuals within the larger seed shadows

(Fig. 3E). Near-neighbor comparisons were lim

ited to seedlings belonging to the same seed

shadow, while random comparisons were made

between individuals selected from each of the seed

shadows. The NAC values for the nearest

neighbor comparison (group size 2) was 1.446. At

group size 20 and group size 60 the NAC values

were 1.426 and 1.425 respectively. The NAC val

ues across all group sizes for the random com

parisons were much lower (1.345). There was lit

tle convergence towards the random NAC value

by the neighbor comparisons. The ratio between

the near-neighbor NAC and the random NAC

was 1.049, 1.060, and 1.062 for seedlings with

group sizes of 2,20 and 60 respectively. The mean

distance between neighbors was near 1 m for

group size 2, 7 m for group size 20 and 11.8 m for

group size 60. There was little relationship be

tween distance and NAC within the seedling shadows (Fig. 3E).

Swartzia simplex var. ochnacea

The four sites analyzed on the FDP (Hamrick &

Loveless 1989) consisted of individuals greater

than 1cm DBH and were separated by approxi

mately 200 m. The FST value among these four

sites was 0.037 (Table 4) indicating that signifi cant genetic heterogeneity (xl = 73.04; P<0.001) occurs among different subdivisions of the FDP.

The mean FIS value within each site was 0.161

(Xi =

25.58; P < 0.001) indicating a significant de

viation from Hardy-Weinberg expectations (Ta ble 5). This FIS value includes, in addition to in

breeding effects, any spatial and temporal genetic

heterogeneity that occurs within these collection

sites.

A total of 686 individuals were sampled from

the WH2 study site. The 0-2 cm diameter class

consisted of 262 individuals while the 2-4 cm

class and individuals larger than 4 cm included

266 and 158 individuals, respectively. There did

not appear to be any distinct clumping of indi

viduals (Fig. 1C). On WH2 different subdivision sizes were used for the three diameter classes to

minimize the variance in FST and FIS due to small

sample sizes. For the 0-2 cm class, FST among the eight 30 m x 30 m subdivisions with more than

15 individuals (Table 4) was 0.021 (x? = 11.00;

P< 0.100). The mean FIS value was 0.103

(X\ = 2.78, P < 0.100) (Table 5). The FST value for the eight 30 m x 30 m subdivisions with more than

15 individuals in the 2-4cm diameter class (Ta ble 4) was 0.019 f?= 10.11; P< 0.100). The

mean FIS for this diameter class was 0.010

(Xi =

0.03; P < 0.750). To obtain adequate sample sizes in the largest diameter class (>4 cm), WH2

was divided into six 36 m x 36 m subdivisions

containing at least 14 individuals. The FST among the subdivisions was 0.031 (xl

= 9.80; P< 0.100)

while the mean FIS within these subdivisions was

0.043 (x? = 0.29; P < 0.500). Values of FST (0.004;

Xi = 5.82; P<0.100) and FIS (0.069; x?

= 3.47; P< 0.100) were also calculated among the three

diameter classes. Since this FIS was based on

individuals from all sections of the plot it may contain a significant Wahlund effect.

The NAC among near-neighbors in the 0-2 cm

diameter class (1.356) was higher than the NAC

based on random comparisons (1.322) (Fig. 4A). The NAC values decreased rapidly as group size

increased to 20. Above group size 20, the NAC

293

A) 0-2cm diameter 1.40

B) 2-4cm diameter

Mean distance

Neighbor

Random

20 30 40

Group size

Mean distance

Neighbor Random

20 30 40

Group size

C) >4cm diameter 1.40

20 30 40 Group size

D) Mean NAC by distance 1.40

0-2cm diameter

2-4cm diameter

>4cm diameter

10 15 20 Mean distance (m)

30

Fig. 4. The relationship of near-neighbor and random NAC values for different group sizes or spatial separation o? Swartzia simplex

individuals belonging to three diameter classes. A. 0-2 cm B. 2-4 cm C. >4 cm D. The NAC values for the three diameter classes

versus distance among individuals being compared. Vertical bars represent + one standard error.

among neighbors was equivalent to the random

NAC. The ratio between the neighbor and the

random NAC for group size 2 was 1.026 while the

ratios for group sizes 20 and 60 were 1.003 and

0.998, respectively. The mean distance from a

central individual to its near-neighbors was 2 m

for group size 2 and increased steadily to 14 m for

group size 60 (Fig. 4B). The NAC for near-neighbor comparisons

within the 2-4 cm diameter class was 1.381 for

group size 2, decreased sharply to 1.359 for group size 10 then leveled off near the random NAC

(1.350) after group size 20 (Fig. 4B). Ratios be

tween near-neighbor and random NAC values

ranged from 1.031 for group size 2, to 1.006 for

group size 10 and 1.004 and 0.997 for group sizes

20 and 60, respectively. The mean distance among

neighbors was about 3.5 m for group size 2, 12 m

for group size 20 and 21m for group size 60

(Fig. 4B). For the largest diameter class (>4cm) NAC values were highest (1.380) when nearest

neighbors were compared (Fig. 4C). At a group size of 10, NAC had decreased to 1.353. Beyond

group size 10, NAC values level off, although they never approach the random values (1.335). The

ratio between random and neighbor NAC values

was 1.037 for group size 2 but decreased to 1.013

by group size 10. The mean distance separating

near-neighbors was 4 m for group size 2 and

steadily increased to 29 m by group size 60

(Fig. 4C). The NAC values for the three diameter classes

294

were related to the mean distances among near

neighbors (Fig. 4D). The NAC for the smallest

diameter class decreased from 2.5 m to approxi

mately 10 m and then leveled off between 10 m

and 15 m. The curves for the two larger diame

ter classes decreased between 2.5 m and 10 m

and then leveled off. Fig. 4D also illustrates that

NAC values of the 0-2 cm diameter class are

somewhat lower than values for the two larger size classes.

Discussion

Significant spatial genetic heterogeneity was ob

served on the FDP for these tropical tree species.

Significant or near significant levels of genetic het

erogeneity were also found at much smaller spa tial scales for the smaller diameter classes of Alseis

and all diameter classes of Swartzia. The largest

spatial genetic heterogeneity, however, was seen

among the seedling shadows of Platypodium adults. This is not surprising since the seedling shadows should consist primarily of sibs. Al

though there was some overlap of seedling shad

ows (Fig. IB) genetic heterogeneity among seed

ling plots was not greatly reduced since seedlings were primarily located near maternal individuals

and away from plot margins. The NAC analyses demonstrate that near

neighbors in the small and intermediate size

classes of each species share more al?eles than

individuals located further apart. The most likely

explanation for this observation is that spatially clustered individuals have at least one parent in

common. Thus, even though there may be con

siderable mixing of seed shadows in the high den

sity species (i.e. Swartzia and Alseis) near

neighbors tend to be more closely related than

randomly paired individuals.

Species with similar densities but different seed

dispersal mechanisms have somewhat different

levels of fine-scale genetic structure. Although we

couldn't compare the fine-scale genetic structure

of Platypodium and Brosimum, the distribution of

seedlings on the FDP indicates that the wind

dispersed Platypodium should have more genetic

heterogeneity among seedling shadows than the

more evenly distributed seedlings of the animal

dispersed Brosimum. The results of the NAC

analysis for Platypodium confirms that near

neighbor pairs of seedlings within the seed

shadow plots have a higher proportion of their

al?eles in common than expected by chance. We

would predict that pairwise comparisons between

the Brosimum seedlings should produce relatively lower NAC values due to the mixture of seedlings from different maternal trees.

At equal densities more structure should exist

within populations of the wind-dispersed Alseis

than for the bird-dispersed Swartzia. This is the

case in the smaller diameter classes where Alseis

has higher NAC ratios than Swartzia (Table 6). The NAC values for Swartzia drop more quickly with increasing group sizes, indicating either that

patches of relatives contain fewer individuals or

are more overlapping in Swartzia than in Alseis.

Comparisons of species with similar seed dis

persal mechanisms but different densities are also

consistent with expectations. At the spatial scale

of the FDP the two species with lower densities, P. elegans and B. alicastrum, have higher FST val

ues indicating that they have more genetic heter

ogeneity among collection sites separated by 100-200 m than the more continuously distrib

uted A. blackiana and S. simplex. This heteroge

neity may be due to the lower number of Platy

podium and Brosimum adults that contribute genes to the different sections of the FDP.

At a smaller scale the existence of patches of

related individuals is not surprising for the low

density species (Platypodium) but is more unex

pected for species with several adults per hectare

(Alseis and Swartzia). Evidently small patches of

related individuals exist in the smaller diameter

classes of these high density species even though there must be considerable overlap of the seed

shadows. In the two species with wind-dispersed

seeds, the lower NAC ratios o? Alseis relative to

those of Platypodium indicate that patches of

Alseis seedlings are derived from more than one

maternal individual. The potential for Alseis seeds

to move more than 100 m (Augspurger 1986) makes the mixture of seed shadows likely. The

genetic structure seen in the seedling (0-2 cm) diameter class of Alseis carried over into the sap

ling diameter class (2-8 cm). The chief difference

in the genetic structure of these two diameter

classes was that the NAC values of the sapling class decreased at lower group sizes and that the

mean distance between near-neighbors was

greater. This is probably due to the loss of indi

viduals from the family patches as the seedling cohorts thin. When Platypodium and Alseis reach

the largest diameter class most of the genetic structure observed in the seedlings has been lost.

This is almost certainly due to the disappearance of the patch structure in the large diameter classes

of these species; as natural demographic pro cesses occur, only one (or perhaps none) of the

members of a seedling patch survive to the larg est size class. As a result, the spatial distribution

of individuals becomes more regular and genetic structure disappears.

A somewhat different picture is seen for Swart

zia. In this species the largest size class (>4 cm) retains substantial fine-scale genetic structure. It

is not clear why Swartzia behaves differently from

Platypodium and Alseis but it may be due to the

more even distribution of individuals within the

three diameter classes. The lack of a T shaped size distribution in WH2 may indicate that there

is less mortality within seedling patches. As a

result, the original family structure may be main

tained in the larger diameter classes.

In Alseis and Swartzia the larger diameter

classes have higher NAC values for both the

near-neighbor and the random comparisons. There are at least two factors that could cause

NAC to increase with size. First, if genetic diver

sity within the study site decreased in the older

age classes both the neighbor and the random

NAC values would increase. Second, if there was

uniform selection for certain multilocus genotypes both NAC values would increase. For Swartzia

and Alseis there is no indication that genetic di

versity is lower or that there is uniform multilocus

selection in the large diameter class. There is

however, evidence that the larger diameter classes

have a higher proportion of heterozygous individ

uals. Inbreeding coefficients (FIS, Table 5) are

295

largest in the smallest diameter class of both spe cies. In Alseis the largest size class has the high est NAC and lowest FIS values. For Swartzia the

major difference in FIS values comes between the

smallest and the two larger diameter classes (Ta ble 5). This is also where differences in NAC val

ues occur. We conclude, therefore, that increases

in heterozygosity associated with size has pro duced an increase in the NAC value.

The calculation of the number of al?eles in com

mon between pairs of individuals has proved to

be a sensitive method to measure fine-scale ge netic structure. The NAC value not only provides an estimate of genetic similarities between indi

viduals but NAC can also be used to determine

the number of individuals within a patch of re

lated individuals and the distances between these

individuals. When the number of individuals in

any diameter class is large our protocol provides an accurate estimate of the difference in genetic

similarity between near-neighbors and randomly chosen individuals.

There are, however, additional ways that the

NAC procedure can be used to describe fine

scale genetic structure. In this paper we com

pared randomly chosen central individuals with

their 1, 3, 5, 9 etc nearest-neighbors. By includ

ing the NAC comparisons from the smaller group sizes in the estimates of the NAC for the larger

group sizes there is a carryover effect that over

estimates mean patch sizes. Actual patch sizes

could be better defined by comparing the central

individual with its five nearest neighbors, then

with its 6-10 nearest neighbors etc. Also, it would

be useful to convert NAC ratios into measures of

genetic relatedness. This was done by Surles et al

(1990) for open-pollinated families of Gleditsia

triacanthos and Robinia pseudoacacia. Since the

expected values for half- or full-sibs vary accord

ing to the genetic diversity in the population these

values should be calculated separately for each

population. Nevertheless, it appears that the NAC

procedure has considerable potential as a mea

sure of multilocus genetic structure in plant pop ulations.

296

Concluding remarks

Considerable fine-scale genetic structure exists in

these tropical tree populations. Furthermore, the

magnitude and spatial distribution of genetic structure is related to the seed dispersal mecha

nisms and adult densities that characterize each

species. Although it is dangerous to generalize from a sample of one species per density and seed

dispersal category, our results indicate that spe cies with wind-dispersed seeds and with lower

densities develop more genetic structure in their

seedlings than species with animal dispersed seeds or higher densities. The effects of seed dis

persal on the establishment of genetically related

near neighbors (i.e. half- and full-sibs) has impli cations for demographic and reproductive pro cesses. For example, in species whose seed dis

persal mechanisms promote the development of

strong patch structure, competition for water, nu

trients, and light will often be among related in

dividuals. In addition, the spread of pathogens

among susceptible seedling cohorts may be facil

itated by the short distances separating related

individuals (Augspurger & Kelly 1984). In species where fine-scale genetic structure established dur

ing seed dispersal persists into the adult genera tion (i.e. Swartzia), the likelihood of inbreeding

will be increased (Hamrick & Loveless 1986).

Biparental inbreeding should be lower in species where patch structure deteriorates with age (i.e. Alseis and Platypodium). Analyses of the breeding structure of tropical trees (e.g. Hamrick & Mu

rawski 1990) coupled with analyses of fine-scale

genetic structure should greatly enhance our un

derstanding of how demographic and evolution

ary processes act to produce the next generation of reproductive adults.

Acknowledgements

We wish to thank the Smithsonian Tropical Re

search Institute for the use of their facilities on

BCI. Thanks are also due to Steve Hubbell and

Robin Foster for all the help and encouragement

they have given over the years. Sue Sherman

Broyles gave valuable technical assistance during the electrophoretic analyses. A. Schnabel and

M.D. Loveless helped with the collection of Alseis

blackiana. D. Santamar?a, R. Perez and C. Chung

provided able field assistance. Funds were pro vided by a grant from the Mellon Foundation to

J.L.H. and by NSF grants BSR 860083 and BSR 8918420.

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