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Biological Journal of the Linncan Socicly (1983), 20: 3-10. With 1 figure
A century of islands:
From Darwin to the Hawaiian Drosophilidae
M. WILLIAMSON
Department of Biology, University of York,
York YO1 5DD, England
Darwin visited c. 50 islands during the voyage of the Beagle, and from this, and his reading, was
impressed by the difficulty of dispersal to pceanic islands, and the descent with modification shown
by forms on such islands. He did not regard isolation as being a normal requisite for speciation. The
general importance of this was not shown until the turn of the century.
In recent years studies on the Drosophilidae of Hawaii have allowed intensive genetical work to
be started on the process of speciation. A quarter to one-third of the world species of-rosophila are
Hawaiian endemics. These have evolved both elaborate courtship patterns, with associated bizarre
morphological changes, and an apparently simple courtship pattern. This second line has
apparently evolved into Scaptomyza on Hawaii. From there, Scaptomyza appears to have spread
round the world, in the first instance largely to other oceanic islands.
Genetical studies on species on isolated islands are one of the most promising areas for
investigating the importance of founder principle, and the processes of speciation.
KEY WORDS-Voyage
of the Beagle - Origin of Species - oceanic islands - dispersal - founder
principle - Hawaiian Drosophilidae - Scaptomyza - speciation.
CONTENTS
. .
Darwin and islands
Developments since Darwin
Hawaiian Drosophilidae .
.
Evolution in Scaptomyza
Conclusion
. . . .
Acknowledgements
. .
References. . . . .
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DARWIN AND ISLANDS
Although this paper is called ‘A century of islands’, because I am going to
discuss our understanding of island biota, particularly their evolution and the
changes in our understanding in the hundred years since Darwin’s death, it
might more appropriately have been called a century and a half of islands. The
reason is that Darwin’s own knowledge and understanding of islands and their
fauna and flora came from the voyage of the Beagle. Everyone knows how
important to Darwin were the observations he made on the Galapagos in the
+
0024-4066/83/050003 08 S03.00/0
3
Q 1983 The Linnean Society of London
4
M. WILLIAMSON
formation of a theory of evolution. So I start with what Darwin saw during
those 4 years, where he went, and the conclusions he drew.
During the voyage of the Beagle, Darwin landed on about 50 islands
comprising 1 ancient continental one which we would regard as oceanic,
(namely North Island, New Zealand), 19 oceanic islands, including 5 islands of
one atoll (though he saw other atolls), high islands with coral reefs, and high
islands without, and more than 27 continental islands. It is not entirely clear
which islands he landed on in Chile (Fitzroy, 1839; Barlow, 1933). Darwin
frequently wrote about the importance of oceanic islands, but he seldom talked
about varieties of other islands. This may reflect the fact that the continental
islands he saw during the voyage included the Falklands and New Zealand,
both of which are hard to fit into any classification.
It is now relatively easy to find out what Darwin said about islands in various
editions of the Origin ( Peckham, 1959; Barrett, Weinshank & Gottleber, 1981),
but the chapter in the Origin which deals particularly with islands is Chapter 12
of the first edition, Chapter 13 of the sixth, the second of the two chapters on
geographical distribution. The chapter starts with discussion of some freshwater
habitats, but after that deals with “On the inhabitants of Oceanic Islands”,
“Absence of Batrachians and of terrestrial Mammals”, “On the relation of the
inhabitants of islands to those of the nearest mainland” and “On colonization
from the nearest source for subsequent modification”. Interestingly, very little of
this chapter appears either in the essay of 1844 or in his manuscript “Natural
Selection” (Stauffer, 1975).
Darwin was impressed both by the difficulty that some organisms had in
reaching oceanic islands, as shown by the absence of Anura and mammals, and
by the fact that inhabitants of islands are related to, but frequently different
from, those of the nearest continent. I t was clear to him, as it is to us, that the
endemic species on an oceanic island mostly come from the nearest continent,
and then evolve their peculiarities on the island, Two examples, the first from
the essay of 1844, illustrate this.
For the first let me quote, “How many islands in the Pacific exist far more like
in their physical conditions to Juan Fernandez than this island is to the coast of
Chile, distant 300 miles; why then, except from mere proximity, should this
island alone be tenanted by two very peculiar species of humming-birds-that
form of birds which is so exclusively American?” (de Beer, 1958: 176). There is
in fact only one endemic species of humming-bird on Juan Fernandez, with two
subspecies on Masatierra and Masafuera, but Darwin is undoubtedly referring
to the first of these subspecies, which was originally described as two species, one
for the male and one for the female, by King in 1831 (Peters, 1945). The world’s
southernmost humming-bird is the green-backed firecrown, Sephanoides sephanoides,
from Chile and south-west Argentina, in which the male differs from the female
by having a scarlet top to its head. In the Fernandez firecrown, S.jernandensis,
the female is very much like the South American species but with extra white on
the tail feathers, but the male is reddish all over (Gooders, 1969: 1462), an
unusual case in which an island form is more strikingly coloured and more
dimorphic than the mainland one. The other example is the Falkland Island
wolf or wolf-like fox in Darwin’s term, Dusicyon australis, which looks rather like
a dog in fox’s clothing, with dog-like legs, but a fox’s head, body and a fox’s tail
ending in a white tip. (The coloured illustration from the ,Zoology of the voyage of
A CENTURY OF ISLANDS
5
the Beagle is reproduced in Moorhead ( 1969).) Dusicyon australis also has enlarged
and rather blunt carnassials (illustrated in Langguth, 1969). Dusicyon is a genus
of South American canids in which many of the species, including the Falkland
Island form, are allopatric.
Both these examples are of allopatric races, sufficiently distinct from their
mainland congeners to have always been called species. They show exactly the
type of evolutionary phenomenon that Darwin found so strikingly exemplified
on oceanic islands. T o quote the Essay again “If we now look to the character of
the inhabitants of small islands, we shall find that those situated close to other
land have a similar fauna with that land, whilst those at a considerable distance
from other land often possess an almost entirely peculiar fauna”.
The other aspect of islands that Darwin was particularly impressed by was the
difficulty of dispersing to them. Both the Origin and, even more, Natural Selection
are concerned with the problems of dispersal, particularly of plants. The passage
in the Origin “If we look to the large size and varied stations of New Zealand,
extending over 780 miles of latitude, and compare its flowering plants, only 750
in number [960 in the 4th edition onwards], with those on an equal area at the
Cape of Good Hope or in Australia, we must, I think, admit there is something
quite independently of any difference in physical conditions has caused so great
a difference in number. Even the uniform county of Cambridge has 874 plants,
and the little island of Anglesey, 764,. . . .” has led some people to suggest that
Darwin had in mind the recent theory of MacArthur & Wilson (1967) in which
the number of species on an island reflect a balance of immigration and
extinction. However, I am in no doubt that Darwin ascribed the smaller
number on islands to the difficulties of dispersal, and that his view was the
correct one that the biota are impoverished because of a lack of equilibrium. In
the first half of that quotation, Darwin talks about equal areas. In the second
half, though, his comparison is vitiated by the species-area effect (Williamson,
1981). For island biota, Darwin fully realized the importance of isolation for
speciation, but he was never convinced that this was a general rule of evolution
(Snow, 1981).
DEVELOPMENTS SINCE DARWIN
The best known, but nevertheless not very important, nineteenth century
development in our understanding of island biotas comes from the work of
Wallace, in his Malay Archipelago (1869) and Island Lijie (1880). Islands have a
never-ceasing fascination for naturalists, and our knowledge of the forms on
them has improved progressively. Wallace was able to talk about oceanic
islands, and discuss the Azores, Bermuda, the Galapagos, St Helena and the
Sandwich Islands (Hawaii). He also talked about continental islands of recent
origin (Great Britain, Borneo, Java, Japan and Formosa), ancient continental
islands discussing Madagascar and various other islands in the Indian Ocean,
and two islands which he called anomalous, Celebes (Sulawesi) and New
Zealand.
Much more important for general biological theory was the development of
what we would now call the theory of allopatric speciation. This continues from
the point discussed in the examples above, in which there are two allopatric
forms, whose genetic relationship is unknown. From there one gets a refusion of
6
M. WILLIAMSON
the ranges, and then it is clear that the two forms have become genetically
isolated and are full species. The genetic isolation of two mendelian populations
is the hallmark of species, and genetic isolation is well known to have arisen by
geographical isolation, in the allopatric mode described above, or by sudden
genetic mechanisms, as in speciation by polyploidy, and, more disputably, by a
variety of other more-or-less well understood mechanisms (White, 1978). The
importance of the allopatric mode was first firmly established, round the turn of
the century, by the group at Tring, namely the second Lord Rothchild who
founded and owned the museum, and his two principal colleagues, Harteret the
ornithologist and Carl Jordan the entomologist (Mayr, 1963). Lord Rothchild
himself was passionately interested in islands, and there are more specimens of
many species of Hawaiian honeycreepers (or finches) at Tring than can be found
now in Hawaii. The theoretical side was particularly Carl Jordan’s work (Mayr,
1955) though Jordan worked primarily with insects of continental range. The
importance of this work and similar studies was not widely appreciated by
academic evolutionists until the publication of Mayr’s Systematics and the Origin of
Species ( 1942).
HAWAIIAN DROSOPHILIDAE
Of all the work that has been done on ecology and evolution on islands in
recent years (Williamson, 1981) the most remarkable has been that on the
Hawaiian Drosophilidae. Here we have hundreds of species on the world’s most
isolated archipelago which have been studied by classical taxonomic methods,
and also both ecologically and genetically. Continental Drosophila larvae are
yeast feeders and their ecology is poorly known. Those in Hawaii are generally
bacterial feeders, and quite a lot is known of the ecology of several species.
Genetically they can be studied by classical segregation methods, by the
examination of polytene chromosomes, by isozymes and by the newer methods
of molecular biology. The specific status of island races may be determinable in
the laboratory. Furthermore, geologists can determine the ages of the islands in
the archipelago, so enabling statements to be made about the speed of
speciation.
O n the latest check list (Wheeler, 1981) there are 1467 described species of
Drosophila (including Ateledrosophila and Nudidrosophila, but excluding
Engiscaptomyza). Of these no fewer than 342, or 23%, are Hawaiian endemics.
Allowing for undescribed species, but not for the probable high rate of
extinction in the Hawaiian lowlands, Williamson (1981) suggests that as many
as one-third of Drosophila species may turn out to be Hawaiian endemics. Many
of these endemic species have remarkably modified antennae, or mouth parts, or
legs, or wings (see Carson et al., 1970; Williamson, 1981; Hardy & Kaneshiro,
1981). Equally remarkably, many of the Hawaiian endemic species show
characters that seem to grade into Scaptomyza, which elsewhere in the world,
although morphologically close to Drosophila, is always clearly distinct from it.
Wheeler’s (1981) list gives 249 species in Scaptomyza and related genera
(Celidosoma, Grimshawomyia, Marguesia and Titanochaeta), of which no fewer than
141 (57%) are Hawaiian endemics.
In one group of about 100 species of endemic Hawaiian Drosophiln, the
picture-wings, Carson and his associates have been able to work out (Carson &
A CENTURY OF ISLANDS
7
Yoon, 1982), with relatively few points of doubt, the phylogeny of the species
from the inversion patterns of the polytene chromosomes. One version of the
phylogeny, and the distribution of the species across the major high islands of
the archipelago, is shown in Williamson (1981 : 186). Many of the speciation
events indubitably involve a movement of a population from one island to
another; it is possible that all speciation events are allopatric, between the major
islands, or between islands in island groups of the archipelago, or between
geographically isolated parts of the same high island (Williamson, 1981). I n any
one phylogenetic line (from arguments that I will develop more fully elsewhere)
the typical time between speciation events is between lo5 and lo6 years.
Speciation is a rare event.
Within the period of 100000 years or more between speciation events, we do
not know, as yet, much about the genetical changes in the genome as a whole,
or the rate and timing of these changes. One interesting question is whether
Mayr’s founder principle may be involved. In his original description (Mayr,
1954) he suggested that it would be a rare event. Nevertheless, the isozyme data,
such as it is, is rather against Mayr’s concept of a genetic revolution (White,
1978; Williamson, 1981). The latest theory of the founder principle (Templeton,
1980) requires a founding population with appreciable genetic variability. Such
a large propagule might well be very rare, but would seem to have enough
genetic variability to adapt readily to a new environment, without invoking any
new principle.
Some of the evolutionary phenomena in Hawaiian drosophilids are shown in
Fig. 1. Evolution seems to have been in two main directions, either to an
elaborate form of courtship with lek-like behaviour or to the simple-appearing
assault courtship, which may nevertheless be as complex as that of continental
Drosophila. Scaptomyza and its relatives show the latter pattern. I n Fig. 1 the
range of size resulting from evolution in Hawaii is notable, as is the fact that
there are large and small flies in both the courtship and the assault sets, though
the most elaborate courtships are found in the largest flies of the picture-wing
groups and antopocerus, while Scaptomyza are typically rather small. The
evolution of a new genus on an oceanic archipelago is notable; even more
notable is the spread of this genus round the world.
EVOLUTION IN SCAPTOMYZA
Table 1 shows the distribution of Scaptomyza subgroups in different parts of
the world. The column headed ‘Other areas’ includes the major continents.
Hawaiian records are listed separately as recognized species, and as records from
individual islands. No genetical studies have been possible as yet in Scaptomyza.
In groups of Hawaiian Drosophila where genetics has been possible, over 90% of
the species have turned out to be single island endemics. Consequently the
island records may be a better indication of the true number of species of
Scaptomyza in Hawaii.
An apparent progression of Scaptomyza round the world in evolutionary time is
apparent in Table 1. Some subgenera are confined to Hawaii. Bunostoma occurs
also in Pacific Oceanic islands and Australia. Other subgenera occur commonly
on oceanic islands but also on the continents, while yet others occur only, as far
M. WILLIAMSON
8
6 body length (mrn 1
0
(Ordinary drosophilid and muscid lengths)
2
4
6
8
I
I
I
I
I
M
I
I
I
I
I
D
I
I
I
I
9
odiastola
phnitibia
I
I
+
I
In
n
-A!!ql
I
I
I
I
c
antopacerus
0
f
ateledrosophila
a
Ill
I
I
I
I
I
I
I
I
From
1
0 robuslo group
b anomoltpes
-*
I
I
I n
I
Unclassified
n
I
I
n
r
I
I
I
I
I
l
I
I
I
While tip scutellurn
I
I
I
II
Modified tarsi
+ pNmaew
A
I
I
I
I
II
+ nudidrmwhila
I
Engiscaptomyza etc.
n
parvo, Exaltoscaptamyza,
Bunasloma, Alloscaptmyza
I
I
I
I
I
I
I
h e n w l d i a , iantalia,
Titanochaeta
2
Figure 1. The length of male Hawaiian Drosophilidae, to the nearest 0.2 mm. The letters D and M
at the top indicate the normal size of drosophilid and muscid flies. There is disagreement about the
origin of the group; see Hardy & Kaneshiro (1981). ‘Engiscaptomyza etc.’ refers to Ensiscaptomyza,
Celidosoma and Grimshawomyia, all sometimes regarded as drosophiloid, sometimes as scaptomyzoid.
All species below these three genera are scaptomyzoid. Data from Hardy (1965) for species
described then or earlier, from the original descriptions, listed in Wheeler (1981), for others.
as is known, on the continents. Trogloscaptomyza is particularly interesting, in
that all species but one have been found on Hawaii, the other one on Tristan d a
Cunha. Evolution seems to follow rare dispersal events, perhaps by seabirds
(Williamson, 1981).
That time is important in the evolution of Scaptomyza is shown in Table 2,
which are the records from the Tristan d a Cunha archipelago in the South
Atlantic. I t can be seen that the number of species is monotonically related to
the age of the islands (and inversely to their area).
A CENTURY OF ISLANDS
9
Table 1. Distribution of Scaptomyza round the world: native species
~~~
Hawaii
Group
parua etc.*
Exalloscaptomyza & Alloscaptomyza
Bunostoma
Trogloscaptomyza etc .t
Parascaptomyza etc. 3
Uncertain subgenera
Scaptomyza sensu strict0
Others8
Total
Island
records
Species
4
Pacific
Oceanic Is.,
N.Z., Australia
Atlantic
Oceanic Is.
0
0
0
10
23
11
142
14
8
109
0
0
0
0
135
0
1
6
3
0
0
14
186
0
0
0
0
11
0
I
10
0
3
0
14
4
0
0
0
0
Other
areas
2
27
40
80
'parva: also Celidosoma and Grimshawomyia.
t Trogloscaptomyza: also Rosmwaldia, Tantalia and
Titanochaeta.
:Parascaptomyza: also Boninoscaptamyza, Lauxanomyza, Macroscaptomyza and Marquesia.
$Others: Dentiscaptomyza,Euscaptomyza, Hemiscaptomyza,Mesoscaptomyza and Metascaptomyza.
Data from: Hardy (1965, 1966) and Wheeler (1981).
Table 2. Scaptomyza in the Tristan da Cunha archipelago
Island
Trogloscaptomyza
Parascaptomyza
Macroscaptomyza
Total species
Age ( lo6 years)
Area (km?)
Tristan
Inaccessible
0
0
0
3
2
2
1
86
Nightingale
Gough
1
0
2
4
2
1
1
5
6
12
7
18
4
2
6
57
Data from: Baird el al. (1965).
CONCLUSION
Studies on Drosophila and Scaptomyza have brought us back to a point of view
which Darwin espoused, namely that isolation on an oceanic island is sufficient
to result in speciation. These flies seem to indicate that genetical isolating
methods arise simply as a consequence of evolution in isolation, though the
genetics of the behaviour and other characteristics involved is still not clear. In
another hundred years it seems likely that the study of evolution on islands will
be a major feature of our improved understanding of speciation.
ACKNOWLEDGEMENTS
I am grateful to Dr H. L. Carson for information and comments on the
Hawaiian Drosophilidae. Part of this paper was presented at the London
Darwin Meeting, 5 July, 1982, and I thank Dr J. S. Jones for organizing that
interesting and economical day.
10
M. WILLIAMSON
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