doi:10.1098/rstb.2008.0118

Review

Colonization and diversiﬁcation of Gala

pagos

terrestrial fauna: a phylogenetic and

biogeographical synthesis

Christine E. Parent

, Adalgisa Caccone

2,3

and Kenneth Petren

Department of Biological Sciences, Simon Fraser University, 8888 University Drive,

Burnaby, Canada BC V5A 1S6

Department of Ecology and Evolutionary Biology, and

Yale Institute of Biospheric Studies, Yale University,

New Haven, CT 06520-8106, USA

Department of Biological Sciences, University of Cincinnati, Cincinnati, OH 45221-0006, USA

Remote oceanic islands have long been recognized as natural models for the study of evolutionary

processes involved in diversiﬁcation. Their remoteness provides opportunities for isolation and

divergence of populations, which make islands remarkable settings for the study of diversiﬁcation.

Groups of islands may share a relatively similar geological history and comparable climate, but their

inhabitants experience subtly different environments and have distinct evolutionary histories, offering

the potential for comparative studies. A range of organisms have colonized the Gala

pagos Islands, and

various lineages have radiated throughout the archipelago to form unique assemblages. This review

pays particular attention to molecular phylogenetic studies of Gala

pagos terrestrial fauna. We ﬁnd

that most of the Gala

pagos terrestrial fauna have diversiﬁed in parallel to the geological formation of

the islands. Lineages have occasionally diversiﬁed within islands, and the clearest cases occur in taxa

with very low vagility and on large islands with diverse habitats. Ecology and habitat specialization

appear to be critical in speciation both within and between islands. Although the number of

phylogenetic studies is continuously increasing, studies of natural history, ecology, evolution and

behaviour are essential to completely reveal how diversiﬁcation proceeded on these islands.

Keywords: adaptive radiation; diversiﬁcation; evolution; phylogeny; phylogeography; speciation

The distribution of the tenants of this archipelago

would not be nearly so wonderful, if, for instance, one

island had a mocking-thrush, and a second island some

other quite distinct genus [.]. But it is the circum-

stance, that several of the islands possess their own

species of the tortoise, mocking-thrush, ﬁnches, and

numerous plants, these species having the same general

habits, occupying analogous situations, and obviously

ﬁlling the same place in the natural economy of this

archipelago, that strikes me with wonder.

(Darwin 1845)

1. INTRODUCTION

Islands have always attracted professional and amateur

students of biology alike. By their very nature, islands

are biologically simpler than continental regions and

therefore provide ideal geographical and historical

settings for the study of colonization and diversiﬁcation

of species. If the timing of their geological formation is

known, such study can be conducted within a deﬁned

time frame. Moreover, if an island is part of an

archipelago, then each island represents a replicate

natural experiment and therefore provides increased

statistical power to test ideas related to patterns

observed and processes inferred about diversiﬁcation.

The Gala

pagos archipelago occupies a unique

position in the history of evolutionary studies, mainly

owing to its importance as a conceptual landmark

(Darwin 1859) and because it continues to shape our

understanding of evolutionary biology (Grant & Grant

2008). Notwithstanding its tropical climate, the Gala

pagos archipelago has been the stage of surprisingly few

animal diversiﬁcations compared with other Paciﬁc

tropical island groups. With only one known exception,

evolutionary radiations on Gala

pagos comprise fewer

than 20 species, and include mainly lineages of land

birds, reptiles and terrestrial invertebrates. Among

vertebrates, the absence of amphibians and the virtual

absence of mammals are particularly striking and nearly

unique among terrestrial island ecosystems.

The goal of this review is threefold. It is (i) to review

literature on Gala

pagos animal groups that have

speciated on the island, (ii) to synthesize the available

evidence in light of classic hypotheses related to

colonization and diversiﬁcation on islands, and (iii) to

suggest future avenues in the study of Gala

pagos faunal

diversiﬁcation and how they can be used to aid in

conservation efforts.

Phil. Trans. R. Soc. B (2008) 363, 3347–3361

doi:10.1098/rstb.2008.0118

Published online 4 September 2008

One contribution of 15 to a Theme Issue ‘Evolution on Paciﬁc

islands: Darwin’s legacy’.

* Author for correspondence ([email protected]).

3347 This journal is q 2008 The Royal Society

2. THE GALA

PAGOS ARCHIPELAGO

(a) Geographical setting

The Gala

pagos Islands are located in the Paciﬁc Ocean,

approximately 960 km west of the South American

coast, straddling the equator at the 90th meridian west

(ﬁgure 1a). The Gala

pagos archipelago is composed of

13 major islands larger than 10 km

, 6 smaller islands,

over 40 islets with ofﬁcial names and many smaller

unnamed islets and rocks, for a total of approximately

8000 km

of land spread over 45 000 km

of water

(Snell et al. 1996). Of these islands, Isabela is the

largest (more than the total area of all the other islands

combined) with an area of 4588 km

and the highest,

with a maximum elevation of just over 1700 m. Isabela

is formed by six volcanoes that are interconnected

mostly by barren lava ﬂows, which may represent a

geographical barrier to dispersal analogous to open

water for terrestrial animal species with low dispersal

capacity such as ﬂightless terrestrial invertebrates.

(b) Geological history

The Gala

pagos Islands are a young, oceanic and

volcanic archipelago. Their geological history is rela-

tively well understood ( Nordlie 1973; Swanson et al.

1974; Bailey 1976; Cox 1983; Hall 1983; White et al.

1993; Geist 1996), with individual islands being

formed as the Nazca plate moved over a hot spot.

However, in contrast to the roughly linear arrangement

by age of the Hawaiian Islands (Price & Clague 2002),

the Gala

pagos Islands are clustered into groups of

similar age ( White et al. 1993). The age of the islands

increases moving eastward along the plate, with the

oldest islands located towards the southeast of the

archipelago. K–Ar age determinations and marine

fossils indicate a maximum age of the oldest land of

the order of 3 Ma, whereas geological plate motion

models set a maximum age of emergence around 4 Ma,

depending on the velocity of the Nazca plate

(Hickman & Lipps 1985; White et al. 1993; Geist

1996; D. Geist 2005–2008, unpublished data; ﬁgure 1a).

The discovery of drowned seamounts east of San

Cristobal extends the time the Gala

pagos have been

available for colonization to at least 14 Ma (Werner et al.

1999). However, the history of island production over

this hot spot could extend back 80–90 Ma, which is the

estimated age of the birth of the Gala

pagos hot spot

(Christie et al. 1992; Hoernle et al. 2002).

The climate of the Gala

pagos Islands is unusually dry

for the tropics and has marked seasonality. Since the

archipelago is so isolated, ocean and wind currents

mostly inﬂuence its climate. There are two main

seasons: the warm season, typically January through

May, and the cool season from June to December. The

warm season is caused by warm ocean currents

sweeping southward from the direction of Panama,

which cause both sea and air temperatures around the

islands to rise. During this time the skies are normally

clear, with occasional heavy showers. During the cool

season, the weather is inﬂuenced by the Humboldt

Current, which brings cold water north from the

Antarctic along the west coast of South America and

then westward through the archipelago, which results

in cooler air temperatures. During the cool season, the

skies are usually overcast, but with little precipitation in

the lowlands. However, many parts of the highlands are

constantly wet at this time owing to a mixture of light

rain and mist. The higher islands have increasingly more

rain at progressively higher elevations and a humid

forest zone exists at 300–600 m on their windward

(eastern) sides. Precipitation is variable in occurrence

and quantity, even in the wet season. The direction of

the wind and oceanic currents changes in response to a

seasonal north–south shift in the Intertropical Conver-

gence Zone (ICZ). On an irregular basis, but typically

once every 3–6 years (Allan et al. 1996), this change in

direction becomes more dramatic and warmer and

wetter seasons occur with potentially 10 times more

than the normal annual rainfall (referred to as El Nin

events). In the cool season during these years, the ICZ

moves greatly to the north of the islands, and the

archipelago falls under the inﬂuence of the cool, dry

wind and cool ocean currents (termed La Nin

a events).

These cyclic changes in climate can have a pronoun-

ced effect on Gala

pagos vegetation (McMullen 1999)

and fauna (Grant & Grant 1993; Grant et al. 2004;

Steinfartz et al. 2007).

Vegetation on Gala

pagos can be separated into six

(or seven) altitudinal zones (Wiggins & Porter 1971;

van der Werff 1979) and the plant species composition

of each zone is a reﬂection of the humidity level of the

zone, with moisture level increasing with elevation

(McMullen 1999). The Gala

pagos ﬂora comprises 749

angiosperm species, of which 216 are endemic to the

archipelago (just under 30%), and 7 of the 192 genera

of ﬂowering plants listed by McMullen (1999) are

endemic to the islands.

(d) E ndemism and diversiﬁcation

Like that of many other isolated oceanic islands, the

Gala

pagos fauna is impoverished and taxonomically

unbalanced when compared with Neotropical source

areas. Owing to their isolation and arid climate, the

Gala

pagos Islands have been successfully colonized by

only a subset of the diverse ﬂora and fauna of the closest

continent. Some lineages that have colonized the

Gala

pagos archipelago have not differentiated from

their continental ancestor (and thus are considered

native) or have differentiated without radiating into

multiple lineages. Both of these scenarios apply to all

sea birds, more than one-third of land bird diversity,

and the great majority of terrestrial invertebrates

(Peck 2001, 2006).

Although relatively few lineages of Gala

pagos

terrestrial fauna have diversiﬁed within the archipelago

(associated with adaptation or not), the resulting

species constitute a large proportion of the terrestrial

vertebrate fauna of the islands (table 1). Bats (two

species) and rats are the only terrestrial mammals that

have naturally colonized the islands, and among

them only the rice rats have diversiﬁed within the

archipelago with 10 recognized species (three extant)

representing three lineages (Clark 1984). Amphibians

have not naturally colonized the islands. Seven

reptile lineages have colonized the Gala

pagos and

at least four diversiﬁed after their arrival, such that

34 of the 37 recognized reptile species are part of

3348 C. E. Parent et al. Review. Diversiﬁcation of Gala

pagos terrestrial fauna

Phil. Trans. R. Soc. B (2008)

multispecies lineages. Of the 30 land bird species,

25 are endemic and 60% of the endemic species belong

to two lineages that have speciated within the

archipelago: Darwin’s ﬁnches (14 species) and Gala

pagos mockingbirds (4 species). By contrast, the

Gala

pagos Islands have approximately 1500 species of

native insects of which only approximately 47% are

endemic. Very few terrestrial insect lineages have led to

multiple species: only approximately 5% of the

approximately 1000 insect genera that have success-

fully colonized the islands have diversiﬁed (Peck 2006)

and those that have diversiﬁed have given rise to

lineages of 20 species or fewer. With 71 described

species, the radiation of Gala

pagos bulimulid land

Darwin (0.4–?)

Wolf (1.0–?)

v. Ecuador

v. Wolf

v. Darwin

v. Alcedo

v. Sierra Negra

v. Cerro Azul

Seymour Norte

Baltra

Plaza Sur

Santa Fe

(2.9–2.9)

Santa Cruz

(1.1–2.3)

Isabela (0.5–0.8)

Floreana (1.5–2.3)

San Cristobal (2.4–4.0)

Española (3.0–3.5)

50 km

PinzÓn

(1.3–2.7)

Santiago (0.8–1.4)

Rabida

(1.3–1.6)

Fernandina

(0.035– 0.07)

Pinta (0.7–?)

Marchena

(0.6–?)

Genovesa

(0.3–?)

Cocos

Galapagos Islands

Ecuador

1°

91° 90° 89°

0°

(a)

100

abingdoni

Pinta

Española

San Cristóbal

Santa Cruz (Cerro Fatal)

Santa Cruz (Cerro Monturra)

Isabela

Santiago

Pinzón

hoodensis

chatamensis

porteri

becki1

becki2

darwini

ephippium

guntheri1

guntheri2

vicina1

vicina2

vicina3

vicina4

vicina5

vandenburghi

microphyes

porteri

Santa Cruz (La Caseta)

0.005 substitutions/site

undescribed*

Floreana

guntheri3

guntheri4

chatamensis*

chilensis

carbonania

denticulata

(b)

B. quitensis

B. sp. 2 (Alcedo, Isabela)

B. sp. 3 (Alcedo, Isabela)

B. tanneri (Wolf, Isabela)

B. darwini (Santiago)

B. blombergi (Santa Cruz)

B. olla (santiago)

B. Perrus 1 (Fernandina)

B. sculpturatus (Santiago)

B. jacobi (Santiago)

B.sp. 9 (Santa Cruz)

B.sp. 6 (Sierra Negra,Isabela)

B.sp.7 (Sierra Negra,Isabela)

B.reibischi (santa Cruz)

B.sp. 8 (Alcedo, Isabela)

B.perrus 2 (Fernandina)

B. tortuganus (Darwin, Isabela)

B. ochsneri (Santa Cruz)

B. wolfi (Santa Cruz)

B. pinzonopsis (Pinzon)

B. indefatigabilis (Santiago)

B. nesioticus (Santiago)

B. sculpturatus (Santiago)

B. akamatus (Santa Cruz)

B. unifasciatus (Floreana)

B. snodgrassi (San Cristobal)

B. amastroides (San Cristobal)

B. exchariferus (San Cristobal)

B. nux (San Cristobal)

B. nux (Floreana)

B. sondgrassi (Española)

B. sp. 1 (Alcedo, Isabela)

100

0.02

100

(0.065527)

(0.209305)

(c)

Geospiza

fuliginosa

Geospiza

fortis

Geospiza

magnirostris

Geospiza

difficilis

Geospiza

scandens

Geospiza

conirostris

Camarhynchus

parvulus

Camarhynchus

pauper

Camarhynchus

psittaccula

Cactospiza

pallida

Cactospiza

heliobates

Pinaroloxias

inornata

Platyspiza

crasstrostris

Geospiza

difficilis

Certhidea

fusca

Certhidea

olivacea

0.006

100

100 100

100

ground finches

tree finches

Cocos

finch

Vege-

tarian

sharp

beaked

warbler finches

(d)

B. Pinzonensis (Pinzon)

undescribed

Figure 1. (a) Map of the Gala

pagos Islands and current hypotheses for the phylogenetic relationships of three Gala

pagos lineages

as follows: (b) giant Gala

pagos tortoises, (c) terrestrial snails and (d ) Darwin’s ﬁnches. (a) Estimated minimum and maximum

geological age for each island are in parentheses (D. Geist 2005–2008, unpublished data). Filled triangles indicate the summits

of the six Isabela volcanoes. The star indicates the location of the hot spot, currently between Fernandina and volcano Cerro

Azul of Isabela (Hooft et al. 2003). (b) Bayesian tree based on mtDNA control region sequences of extant and extinct Gala

pagos

tortoises. Extinct taxa are asterisked. Placement of the three lineages on Santa Cruz is indicated with an arrow, and the pictures

exemplify their different carapace morphologies. Redrawn from Russello et al. (2005).(c) Best maximum likelihood

phylogenetic tree based on combined mtDNA COI and nDNA ITS1 sequence data. Two long branches were shortened and

their actual lengths are reported in brackets below them. The snail outlines are roughly proportional to actual size. Species on

older islands connect at deeper nodes, with a signiﬁcant negative relationship between the depth of the clade encompassing an

islands’ species and the island’s age. For each tree, numbers above branches are Bayesian posterior probabilities. Maximum

likelihood bootstrap proportions more than 50% are given below branches for b.(d ) Phylogenetic tree of Darwin’s ﬁnches

estimated from cytochrome b sequences and neighbour joining (Petren et al. 2005). There is signiﬁcant genetic structure and

paraphyly among populations of sharp-beaked ground ﬁnches and warbler ﬁnches, but lack of resolution among the

phenotypically distinct species of ground ﬁnches and tree ﬁnches. Photographs are proportional to actual size.

Review. Diversiﬁcation of Gala

pagos terrestrial fauna C. E. Parent et al. 3349

Phil. Trans. R. Soc. B (2008)

snails is the most spectacular in the fauna in terms of

species number (Chambers 1991; Parent & Crespi

2006). None of the other nine land snail genera that

have colonized the islands have diversiﬁed into more

than four species (Smith 1966) and preliminary

phylogenetic evidence suggests that the four species of

the genus Succinea are descendants of at least two indep-

endent colonizations (B. S. Holland 2008, personal

communication). Ta b le 2 summarizes the within-

archipelago diversiﬁcation of Gala

pagos terrestrial

fauna, and in the following sections we will describe

the main diversiﬁcation patterns.

3. ORIGINS AND AGE OF GALA

PAGOS FAUNA

(a) Origin of the fauna

The terrestrial Gala

pagos fauna that has diversiﬁed on

the islands generally has close relatives on the South

American continent. This is the case for Gala

pagos

tortoises, which are closely related to the smaller

bodied Geochelone chilensis, or Chaco tortoise, from

South America (Caccone et al. 1999). The diversity of

Gala

pagos lava lizards (Microlophus spp.) is the result of

two independent colonizations, both from the west

coast of South America (Wright 1983; Kizirian et al.

2004; Benavides et al. 2007). Likewise, Wright (1983)

suggested that the leaf-toed gecko (Phyllodactylus)

diversity stems from more than one colonization from

South America; however, this suggestion has not been

tested with phylogenetic analyses including possible

mainland relatives.

The two land bird lineages that have diversiﬁed on

Gala

pagos do not necessarily bear a strong relationship

to relatives on the adjacent Ecuadorian mainland:

Darwin’s ﬁnches appear to be most closely related to

grassquits (Tiaris) and their allies, a group with a wide

distribution throughout Central and South America that

has undergone a similar radiation in the Caribbean (Sato

et al. 2001; Burns et al. 2002). The closest living relatives

of Gala

pagos mockingbirds appear to be those currently

found in North America, northern South America and

the Caribbean, rather than the geographically nearest

species in continental Ecuador (Arbogast et al. 2006).

The endemic subspecies of the yellow warbler (Dendroica

petechia aureola) probably migrated from Latin America,

not North America, but it shows little evidence of

divergence within Gala

pagos (Browne et al. submitted).

Several other taxa in Gala

pagos (e.g. ﬂamingos,

isopods, snakes, moths) show biogeographical afﬁnities

with populations in the Caribbean ( Thornton 1971;

Grehan 2001); but these proposed afﬁnities have not

been tested with molecular phylogenetic analyses.

The geographical origin of very few terrestrial

invertebrate groups has been inferred with certainty.

This gap in our knowledge is mostly because few

detailed data exist on the continental distributions of

possible sister species of Gala

pagos endemics. Schmitz

et al. (2007) suggested that the source of the Gala

pagos

microlepidopteran genus Galagete is probably coastal

South America, but this remains to be tested. Likewise,

based on morphological afﬁnities, Gala

pagos bulimulid

snails seem to be most closely related to continental

South American bulimulids (Breure 1979). One must

be cautious though, as the South American fauna is

rather poorly known, especially the invertebrate

fauna, and it is possible that sister clades of Gala

pagos

lineages have recently become extinct, undergone range

shifts or simply have yet to be identiﬁed. A striking

example of this lack of knowledge is the genus ofﬂightless

beetles Stomion, whose non-Gala

pagos closest relative is

unknown (Finston & Peck 2004).

(b) Age of the fauna

Colonization events have occurred over the last 3–4 Ma

during the existence of the present islands, and might

have happened earlier when now sunken islands were

above sea level. The presence of several drowned

seamounts on the Carnegie Ridge east of the Gala

pagos

(Christie et al. 1992) suggests that earlier volcanic

islands may have served as stepping stones for

colonization by some of the terrestrial fauna. Because

divergence times estimated directly from molecular data

require independent calibration, all current dating

methods require that speciﬁc assumptions be made

before inferring any divergence time. These assump-

tions typically are related either to rates of molecular

evolution (molecular clock hypothesis, local clocks

models) or both rates and times (penalized likelihood,

Bayesian methods). Among the few Gala

pagos taxa for

which such estimations have been attempted, the

divergence time between the mainland ancestor and

island relatives seems in some cases to be older than the

age of the existing emerged islands. The divergence

between G. chilensis and the Gala

pagos tortoise lineage

probably occurred 6–12 Ma, before the origin of the

oldest extant Gala

pagos island (Caccone et al. 1999).

However, the closest extant relative does not necessarily

Table 1. Species diversity of Gala

pagos terrestrial animals. (For each group, the numbers of native species in the following

categories are given: undifferentiated from non-Gala

pagos relatives (indigenous): differentiated from a non-Gala

pagos relative

but have not diversiﬁed within Gala

pagos (single-species endemic); diversiﬁed within Gala

pagos (multiple-species endemics

with number of independent within-Gala

pagos lineages in parentheses); and total recognized native species. Numbers are not

available for all terrestrial invertebrate groups; only data for beetles and land snails are reported.)

taxonomic group indigenous single-species endemic

multiple-species endemic

(number of lineages) total

mammals 1 1 10 (1) 12

land birds 5 7 18 (2) 30

reptiles 2 3 36 (5) 41

beetles 108 108 164 (42) 380

land snails 0 5 82 (5) 87

3350 C. E. Parent et al. Review. Diversiﬁcation of Gala

pagos terrestrial fauna

Phil. Trans. R. Soc. B (2008)

Table 2. Summary of diversiﬁcation of the terrestrial fauna of Gala

pagos, with the number of species per lineage that evolved on the archipelago, number of colonizing species from which they

evolved, their probable geographical origin, as well as molecular estimates (millions of years) of the initial divergence within the lineage and the temporal window of divergence from their

ancestor, whether a lineage follows the progression rule pattern (see text), whether multiple species are found within an island or volcano or whether there is evidence that the lineage is an

adaptive radiation. (For invertebrates, only lineages with 10 species or more are listed.)

class taxa

number of

species or

subspecies

phylogeny

available?

number of

colonization

events

geographical

origin

time of initial

divergence

within

Gala

pagos

(Ma)

divergence

time with

closest extant

lineage (Ma)

progression

rule?

multiple

species per

island or

volcano?

adaptive

radiation? source

Mammalia rice rats

(Oryzomys,

Nesoryzomys,

Megaoryzomys)

at least 8 no 3? North, Central,

and South

America

? ? ? on Santa Cruz,

Isabela and

Fernandina

no Clark (1984)

Reptilia Gala

pagos

giant tortoise

(Geochelone nigra)

15 (11

extant)

yes 1 South America 1.5–2.0 6.0–12.0 yes on Santa Cruz

and Isabela

may be Caccone et al.

(1999, 2002),

Beheregaray

et al. (2004),

Russello et al.

(2005) and

Cioﬁ et al. (2006)

lava lizards

(Microlophus)

9 yes 2 South America 1.4

10.2

yes no, one

island and

one species

Wright (1983),

Lopez et al. (1992)

2.0–2.7

#,a #

Benavides et al.

(2007)3.6–4.0

#,b

snakes (Philodryas,

Alsophis)

3 no 3? South America

and Caribbean

? ? ? yes ? Thomas (1997) and

Grehan (2001)

leaf-toed geckos

(Phyllodactylus)

6 yes 3? South America ? 8.9 yes on San

Cristo

bal

only

no Wright (1983)

marine

(Amblyrhynchus

cristatus)and

land (Conolophus

spp.) iguanas

1 (marine)

2 (land)

yes 1? South America O10 !2 yes land iguana:

on V. Wolf

(Isabela)

may be Wyles & Sarich

(1983),

Rassmann (1997),

S. Glaberman et al.

2005–2008

(unpublished data),

G. Gentile, et al.

2005–2008

(unpublished data)

and S. Steinfartz

et al. 2005–2008

(unpublished data)

(Continued.)

Review. Diversiﬁcation of Gala

pagos terrestrial fauna C. E. Parent et al. 3351

Phil. Trans. R. Soc. B (2008)

Table 2. (Continued.)

class taxa

number of

species or

subspecies

phylogeny

available?

number of

colonization

events

geographical

origin

time of initial

divergence

within

Gala

pagos

(Ma)

divergence

time with

closest extant

lineage (Ma)

progression

rule?

multiple

species per

island or

volcano?

adaptive

radiation? source

Aves Darwin’s ﬁnches

(Geospiza,

Camarhynchus,

Cactospiza,

Platyspiza,

Certhidea)

14 yes 1 South America/

Caribbean

1.6 2.0–2.3 no yes yes Sato et al. (2001),

Burns et al. (2002)

and Petren et al.

(2005)

mockingbirds

(Nesomimus)

4 yes 1 North America/

Caribbean

? 0.6–5.5 yes no no Arbogast et al. (2006)

Insecta Galagete

microlepidoptera

12 yes 1 South America 2.9–3.7 ? no yes no Schmitz et al. (2007)

Galapaganus

weevils

10 yes 1 South America 10.7–12.1 7.2 no yes no Sequeira et al. (2000)

Stomion darklings 12 yes 1 ? ? ? ? yes no Finston & Peck

(1997, 2004)

Ammophorus 12 no 2? South America ? ? ? yes ? Peck (2006)

Philatis 20 no 1 South America? ? ? ? yes ? Peck (2001)

Scaphytopius 17 no 2? ? ? ? ? yes ? Peck (2001)

Oliarus 12 no 1 ? ? ? ? yes ? Peck (2001)

Pterostichus 12 no 2? South America? ? ? ? Desender et al. (1992)

and Peck (2006)

Dagbertus ? on Santa

Cruz,

San-

tiago

and

Isabela

5? ? ? ?Peck (2001)

Blapstinus ? yes 3? South America? ? ? ? Peck (2006)

Gastropoda Bulimulus

land snails

? yes 1 South America ? ? yes Breure (1979) and

Parent & Crespi

(2006)

yes yes

Microlophus ‘Eastern radiation’.

Microlophus ‘Western Radiation’.

3352 C. E. Parent et al. Review. Diversiﬁcation of Gala

pagos terrestrial fauna

Phil. Trans. R. Soc. B (2008)

represent the direct ancestor, which could have been,

and perhaps was, a now extinct lineage of mainland

giant tortoises. Thus, the date of the oldest divergence

within the Gala

pagos lineage probably provides a

more accurate estimate of the minimum time since

colonization. The oldest node within the Gala

pagos

tortoise radiation is a little more recent than the oldest

islands and the molecular divergence time for the

southern Isabela clade is less than 500 000 years,

which agrees with estimates of the island’s age

( Naumann & Geist 2000; Caccone et al. 2002;

Beheregaray et al. 2003b, 2004).

Data from cytochrome b mitochondrial DNA

(mtDNA) sequences indicate a time for the divergence

of the land and marine iguana lineages of less than

10 Ma (Rassmann et al. 1997), which precedes the

origin of the emerged islands. This suggests that they

ﬁrst colonized the now submerged islands and then

colonized the current islands as they emerged. Genetic

work on both land and marine iguanas is revisiting

this dating (S. Glaberman, D. Lanterbecq, S. Steinfartz,

C. Marquez, K. Dion, T. Hanley, A. Caccone 2005–

2008, unpublished data; G. Gentile, M. Milinkovitch,

A. Fabiani, C. Marquez, H. L. Snell, H. M. Snell &

W. Tapia 2005–2008, unpublished data), which was

basedonanoverallmtDNArateof2%Myr

extrapolated from bovid data.

Colonization of the Gala

pagos by ancestors of

Darwin’s ﬁnches has been estimated at 1.6–2.3 Ma

(Sato et al. 2001), well within the age of the

present islands.

Galapaganus beetles are estimated to have diverged

from their closest living, mainland relative over 7 Ma,

based on both an intrinsic (Sequeira et al. 2008)and

extrinsic clock (Sequeira et al. 2000). However, most

DNA derived estimates of the timing of interisland

colonization and within-island diversiﬁcation are

consistent with the geological formation of the islands

(Sequeira et al. 2008). The earliest divergence time

within the endemic Gala

pagos lepidopteran Galagete

radiation was estimated at 3.3 Ma, within the time that

the present islands were available for colonization

(Schmitz et al. 2007).

For other Gala

pagos lineages, it is not possible to

estimate the time of divergence from their closest

relatives because there is no reliable molecular clock

for the taxonomic group and/or genes in question

(Parent & Crespi 2006), or the relevant continental

biota is so poorly known that their close relatives cannot

be identiﬁed (table 2). Another possibility is that the

closest extant relative outside the archipelago does not

necessarily represent the direct ancestor of the insular

lineage, which could be extinct (Emerson 2002).

4. TIMING AND SEQUENCE OF COLONIZATION

AND SPECIATION

The sequence of colonization and speciation within

the archipelago can be inferred by comparing phyloge-

netic information on a lineage with the geological ages of

the islands. The most commonly predicted and tested

colonization scenario is a movement from old to young

islands, suggesting that successful intraarchipelago

colonization is more likely to occur on recently formed

islands with unoccupied niches (Brooks & McLennan

1991). This pattern, often referred to as the progression

rule (Wagner & Funk 1995), has been observed in a range

of lineages and island systems (Fleischer et al. 1998; Juan

et al. 2000). On Gala

pagos, this implies a diversiﬁcation

sequence from southeast to northwest, paralleling the

geological formation of the islands. The Gala

pagos

archipelago is formed by geographical clusters of islands

of similar age (White et al. 1993)andthereforeifthe

progression rule applies, species formation should also

occur in ‘clusters’ and not necessarily match perfectly the

sequence from old to young islands.

The historical biogeographical scenarios proposed for

Gala

pagos endemic organisms based on phylogenetic

hypotheses suggest inconsistent relationships between

population diversiﬁcation and island formation across

lineages. The Gala

pagos giant tortoises lineage is among

the best-studied cases of diversiﬁcation on the islands,

with species-level phylogenetic analyses based on

multiple mtDNA markers (Caccone et al. 1999, 2002),

as well as population level demographic history and

population structure analyses based on both mtDNA

(Beheregaray et al. 2004; Russello et al. 2007a)and

several microsatellite markers (Beheregaray et al.

2003a,b; Cioﬁ et al. 2006). Although the lineage of

giant tortoises does not follow a strict linear migration

from older to younger islands, the species-level phyloge-

netic pattern uncovered from mtDNA data suggests that

giant tortoises diversiﬁed approximately in parallel to

island geological formation (Caccone et al. 2002;

ﬁgure 1b). Furthermore, estimation of population-level

genetic diversity, population divergence and recent

demographic history of Gala

pagos giant tortoises based

on mtDNA revealed a pattern of lineage sorting

consistent with the temporal formation of the archipelago

(Beheregaray et al. 2004). Indeed, tortoise species from

older islands have exclusively endemic haplotypes that

deﬁne divergent monophyletic clades, whereas taxa

from younger islands (Isabela, in particular) have

haplotypes shared among lineages on different volcanoes

and which exhibit a recent history of coalescence

(Beheregaray et al. 2004). One of the two lineages of

Gala

pagos lava lizards has also diversiﬁed in concordance

with the geological formation of island clusters of similar

age (Kizirian et al. 2004).

In a population genetic study of 22 populations of

marine iguanas (Amblyrhynchus cristatus), Rassmann

et al. (1997) found that the mtDNA cytochrome b

marker had a signature of population differentiation

concordant with geographical isolation of populations

across the archipelago. However, data from three

nuclear microsatellite loci indicated relatively high

levels of gene exchange among populations (mean

Z0.1), contradicting the mtDNA pattern. This

discrepancy was suggested as being due to sex-biased

dispersal, with higher interpopulation dispersal in

males than females (Rassmann et al. 1997). A current

analysis of the population structure of marine iguanas

based on 13 microsatellite loci, however, depicts a very

different picture in which most island populations

represent different genetic clusters (Steinfartz et al.

2007; S. Steinfartz, D. Lanterbecq, C. Marquez &

A. Caccone 2005–2008, unpublished data). A compa-

nion analysis using mtDNA control region data reveals

Review. Diversiﬁcation of Gala

pagos terrestrial fauna C. E. Parent et al. 3353

Phil. Trans. R. Soc. B (2008)

three main mtDNA lineages, as follows: one on the

eastern and central islands, one restricted to the northern

and western islands and one that spans from east

to west (S. Glaberman, D. Lanterbecq, S. Steinfartz,

C. Marquez, K. Dion, T. Hanley & A. Caccone

2005–2008, unpublished data). The evolutionary

relationships among these groups are unclear owing to

shallow levels of divergence, as in the cytochrome b data.

Thus, the patterns of island colonization are not as well

deﬁned as for the tortoises. It is clear, however, that the

lineage occupying the northern and western regions of the

archipelago is the product of a recent expansion based on a

unimodal distribution of pairwise differences

between individuals as well as a high abundance of low-

frequency haplotypes. This conclusion ﬁts with the

overall younger age of the western islands.

Gala

pagos mocking birds were inferred to follow the

progression rule (Arbogast et al. 2006). By contrast,

Darwin’s ﬁnches show limited evidence of diversiﬁca-

tion closely associated with the geological formation of

the islands. Grant & Grant (2008) suggested that the

radiation of ﬁnches unfolded with an increase of types

of species with change in climate and increased habitat

diversity, associated with an increased number of

islands. However, there is no clear evidence suggesting

that the number of islands has increased through

time. Nevertheless, divergence time within this lineage

is not associated with the age of the islands where the

species are found, perhaps a result of considerable

interisland dispersal.

A progression rule pattern has been inferred for

Gala

pagos bulimulid land snails (Parent & Crespi 2006;

ﬁgure 1c). By contrast, Gala

pagos ﬂightless weevils

(genus Galapaganus) do not follow the progression rule.

Phylogenies based on mtDNA (Sequeira et al. 2008)or

mtDNA combined with nDNA (Sequeira et al. 2008)

indicate that colonization and diversiﬁcation in this

lineage are linked to geological history in a more complex

scenario. For example, Galapaganus williamsi,which

occurs only on Isabela, coalesces at the deepest node of

the phylogeny, while species from the oldest islands of

Espan

ola and San Cristobal are shallower in the

phylogenetic tree. The Microlepidoptera genus Galagete

(12 species) is another example in which the progression

rule fails to explain phylogeographical patterns of

diversiﬁcation. Species connecting at the deepest node

are not found on the oldest islands and the sequence of

colonization and speciation does not follow the geological

formation of the islands, but rather a stochastic

colonization scenario (Schmitz et al. 2007).

In general, the diversiﬁcation sequence in Gala

pagos

terrestrial faunal groups seems to follow the pro-

gression rule, with the more vagile lineages constituting

the exception (Gala

pagos ﬁnches, Galagete lepidopter-

ans and Galapaganus weevils).

5. THE GEOGRAPHICAL MODE OF SPECIATION

In an insular context, speciation can happen between or

within islands. If colonization rate between islands is

high and individuals interbreed among island popu-

lations, these populations will effectively be part of

the same gene pool. However, ongoing but low levels

of gene ﬂow do not constrain local adaptations of

Darwin’s ﬁnch (Petren et al. 2005) or lava lizard

(Jordan et al. 2005) populations on islets peripheral to a

main island. Lineages that have recently colonized the

islands might not have had the time to differentiate

within the archipelago. The Gala

pagos hawk is thought

to have diverged from its continental sister clade less

than 300 000 years ago, and populations from different

islands are genetically very similar (Bollmer et al.

2006). However, mitochondrial and minisatellite data

indicate a general pattern of rapid population expan-

sion followed by genetic isolation of hawk populations,

suggesting that this lineage is in the earliest stages of

further divergence (Bollmer et al. 2006). Genetic

analysis of the Gala

pagos hawks’s ischnoceran louse

may shed further light on the cryptic evolutionary

history of its host (Whiteman et al. 2007).

(a) Speciation between islands

If colonization rate between islands is low, one would

expect to ﬁnd a pattern of genetic structuring among

island populations, potentially leading to differentiated

species that are single island endemics. Rassmann

et al. (1997) initially proposed that marine iguana

populations across the archipelago showed very little

divergence but ongoing work suggests that most

island populations have considerable levels of

genetic differentiation (S. Steinfartz, D. Lanterbecq,

C. Marquez & A. Caccone 2005–2008, unpublished

data). Gala

pagos giant tortoises have diverged to form

15 taxa, 11 of which are extant. Their taxonomic

status is still in ﬂux. Some authors consider them

different subspecies (Pritchard 1996), while others

refer to them as species owing to their genetic

distinctiveness (Powell & Caccone 2006; Russello

et al. 2007a). Espan

ola, San Cristobal, Pinzo

Santiago and Pinta each has only one named species;

San Cristobal had two distinct populations but one is

now extinct (Caccone et al. 2002; Russello et al.

2007a). Isolation among islands has promoted specia-

tion in the two independent lineages of lava lizards

(Kizirian et al. 2004; Benavides et al. 2007). Using

microsatellite markers, Jordan & Snell (2008) have

tested the hypothesis that genetic drift in isolation has

caused the differentiation of Gala

pagos lava lizards on

12 islets that were probably connected to the larger

island of Santa Cruz during the Late Pleistocene.

They found strong genetic differentiation among

island populations, a positive correlation of genetic

diversity with island size, no relationship between

genetic and geographical distance and a strong

negative correlation between heterozygosity and

measures of genetic differentiation. They concluded

that overwater dispersal is rare and further differen-

tiation of lava lizards may be prevented by island

fusion during periods of lower sea level. The land

iguanas (Snell et al. 1984; Rassmann 1997) and the

mocking birds (Arbogast et al. 2006) also have at

most one species per island, but the relative contri-

butions ofselection and drift to differentiation remain

unclear. Recent work on the two Gala

pagos land

iguanas, Conolophus subcristatus and Conolophus

pallidus (G. Gentile, M. Milinkovitch, A. Fabiani,

C. Marquez, H. L. Snell, H. M. Snell & W. Tapia

2008–2008, unpublished data), based on mtDNA

3354 C. E. Parent et al. Review. Diversiﬁcation of Gala

pagos terrestrial fauna

Phil. Trans. R. Soc. B (2008)

sequence data, conﬁrms the genetic discontinuities

between the populations of C. subcristatus from the

western (Fernandina and Isabela) and central (Santa

Cruz, Baltra, Seymour and Plaza Sur) islands. This

pattern seems to parallel that of their sister taxon, the

marine iguanas, in which there is clear genetic

differentiation between eastern and western islands

(S.Glaberman,D.Lanterbecq,S.Steinfartz,

C.Marquez,K.Dion,T.Hanley&A.Caccone

2005–2008, unpublished data; S. Steinfartz, D. Lanter-

becq, C. Marquez & A. Caccone 2005–2008, unpub-

lished data). The level of differentiation between the two

C. subcristatus groups is only slightly lower than that

between the two species (C. subcristatus and C. pallidus).

Darwin’s ﬁnches show limited evidence of speciation

on different islands. The larger central islands contain

largely the same suite of 9–10 species, many of which

also occur on several smaller and peripheral islands

(Grant 1999). Several phylogenetic analyses have

revealed little resolution among six species of tree

ﬁnches and ﬁve species of ground ﬁnches (Freeland &

Boag 1999; Sato et al. 2001; Petren et al. 2005;

ﬁgure 1d ). A combination of factors is probably

responsible for this, including the recent origin of

many species, the homogenizing effects of hybrid-

ization (Grant et al. 2004) and interisland dispersal

(Petren et al. 2005). Allopatric speciation has been

inferred between the small (Geospiza scandens)and

large (Geospiza conirostris) cactus ﬁnches, although

both populations of large cactus ﬁnches are more

closely related genetically to different populations of

small cactus ﬁnches than they are to one another.

The warbler ﬁnches (Certhidea olivacea and Certhidea

fusca) were believed to be the same species, until

studies showed different subsets of islands to harbour

two different species that are more genetically distinct

than any other species in the entire group (Petren

et al. 1999; Tonnis et al. 2005). There is pronounced

morphological divergence between-island populations

of several species of Darwin’s ﬁnches. Some of these

differences are paralleled by substantial genetic

differences (Geospiza difﬁcilis, G. scandens/G. conirostris),

while in other cases, genetic differences are minimal or

are not correlated with morphological or geographical

divergence (Geospiza fortis/Geospiza magnirostris; Petren

et al. 1999, 2005). Recent studies suggest interisland

movements of Darwin’s ﬁnches may not be as rare as

previously suspected (Petren et al. 2005; Tonnis et al.

2005). Morphological differences among island popu-

lations may therefore not be as much evidence of isolation

from gene ﬂow as previously thought, but rather evidence

of differing selective regimes and local adaptation in the

presence of gene ﬂow. Theoretically, low levels of gene

exchange may promote local adaptation under

some conditions (Whitlock & Phillips 2000). The

warbler ﬁnches (C. fusca and C. olivacea)appearto

conform to an allopatric mode of speciation, being clearly

separated on different subsets of islands. However, the

occurrence of some very widely distributed C. fusca

haplotypes suggests that speciation was not driven by

geographical isolation and limited dispersal. Other

factors, such as habitat or natural selection against

immigrants, may have limited genetic exchange and

allowed speciation to occur (To nn i s et al. 2005).

Terrestrial invertebrates often have low dispersal

ability (especially ﬂightless groups), so single island

endemics would be expected. The ﬂightless beetle

genus Neoryctes includes four single island endemic

species, each restricted to the moist highland zone

of the island on which it occurs (Cook et al. 1995). The

microlepidopteran genus Galagete has a complex pattern

of diversiﬁcation. Some of the species are single-island

endemics, others are found on multiple islands, and two

occur on 10 and 11 islands (Schmitz et al. 2007). The

inference of the geographical mode of speciation from

the phylogeny is problematic, mainly owing to the

wide distribution of most of its taxa. Little is known

of the ecology of Galagete (Schmitz et al. 2007), which

makes it difﬁcult to infer ecological or habitat shifts.

In sum, patterns of speciation between islands tend

largely to reﬂect a combination of dispersal capability

and habitat suitability. Less vagile taxa show more

pronounced genetic structure among island popu-

lations. They are more prone to longer periods of

absence from suitable islands as a result of extinction.

More vagile taxa show little differentiation among

subsets of islands, but may be absent from islands with

apparent suitable habitat. Several taxa show non-

overlapping distributions among subsets of islands.

In these cases, co-occurrence may be limited by

dispersal, but also by the presence of other similar

species. The possibility of occasional gene exchange

between islands that would create loose evolutionary

connections among differentiated populations remains

largely unexplored.

(b) Speciation within islands

In addition to island isolation, other physical features

of islands can inﬂuence the mode of diversiﬁcation in

an archipelago. Island area and elevation are positively

correlated in many island groups and are prime

determinants of moisture and island habitat diversity.

Greater habitat diversity provides the potential for

within-island diversiﬁcation, but also increases the

chances that a new colonist will ﬁnd a suitable habitat.

Once a particular lineage has colonized an island, it can

speciate within that island either by adapting to

different habitats, commonly referred to as ecological

speciation (Schluter 2000), or by allopatric speciation if

an island is large enough for populations to become

isolated by geographical or topological means (volca-

noes, barren lava, inhospitable habitat, etc.). The

strength of the effect of island area depends not only

on geography and topology but also on the dispersal

ability of the organisms, being strongest for animals

with low dispersal ability and specialized ecological

requirements. The low dispersal ability of the giant

tortoises is a good example, with four species on

Isabela, one on each major volcano. Isabela probably

started as separate island volcanoes that then

merged. The volcanoes are now separated by lava

ﬁelds, which are a formidable obstacle to tortoise

movement. It is therefore possible that their popu-

lations were isolated for 400 000 years, and then

experienced limited mixing (over the lava ﬁelds) for

the past 100 000 years once the volcanoes were

connected. mtDNA and nDNA data support the

genetic distinctiveness of the three species living on

Review. Diversiﬁcation of Gala

pagos terrestrial fauna C. E. Parent et al. 3355

Phil. Trans. R. Soc. B (2008)

the central and northern volcanoes (Alcedo, Darwin,

Wolf; Caccone et al. 2002; Beheregaray et al. 2004;

Cioﬁ et al. 2006, in press; Russello et al. 2007a).

However, genetic divergence and similarities among

populations on the southern volcanoes (Cerro Azul,

Sierra Negra) do not support the taxonomic subdivi-

sions (Cioﬁ et al. 2006) that were previously suggested

based on morphology ( Fritts 1984; Pritchard 1996).

The taxonomic assignment of tortoise populations on

Santa Cruz has been contentious. There are at least

three lineages that are as genetically distinct from

each other as from lineages on other islands, being

connected only through the deepest nodes in the

molecularly based tree (Russello et al. 2005). Shell

shape (domed versus saddlebacked carapace) is the

most distinctive phenotypic difference among giant

tortoise populations and has been associated with

habitat differences. The ancestral state of this character

in Gala

pagos is probably domed (Caccone et al. 2002;

Russello et al. 2005) and recent DNA data from extinct

taxa suggest that the saddleback morphology arose

independently more than once (Russello et al. 2005;

Poulakakis et al. 2005–2008, unpublished data).

However, the role of selection and developmental

constraints in the diversiﬁcation of Gala

pagos giant

tortoises remains to be clearly determined. Research

using novel ﬁeld friendly three-dimensional imaging

techniques and morphometric methods is addressing

such issues (Chiari et al. in press).

Within-island divergence has been suggested as a

mode of speciation for Darwin’s ﬁnches. Divergence

occurs along an elevational gradient in small ground

ﬁnches on Santa Cruz (Kleindorfer et al. 2006).

Geospiza conirostris on Genovesa showed an ephemeral

tendency to mate assortatively according to similarities

in beak shape and song (Grant & Grant 1989).

Assortative mating according to beak size occurs within

populations of medium ground ﬁnches on Santa Cruz,

although this tendency appears to be signiﬁcantly

reduced by human activity (Hendry et al. 2006) and

wet conditions, when competition is also presumably

reduced (Huber et al. 2007). Sympatric speciation has

yet to be convincingly demonstrated in birds on islands

such as the Gala

pagos that are smaller than 10 000 km

(Coyne & Price 2000), and so it seems unlikely that any

of these situations will result in complete speciation.

Lack (1947) proposed a model for within-island

species build-up of Darwin’s ﬁnches that relied on

limited dispersal between islands to create initial diff-

erences in allopatry, followed by rare colonization,

establishment of secondary contact and further differ-

entiation in sympatry as a result of resource compe-

tition and character displacement. This model has in

principle been adapted to account for faunal commu-

nity build-up in a wide variety of systems including

Gala

pagos taxa. Despite the apparent lack of isolation

between ﬁnch populations on different islands (Petren

et al. 2005), Lack’s model of faunal build-up may

still apply. Immigrants that normally interbreed with

residents may on rare occasions form distinct, repro-

ductively isolated populations, depending on environ-

mental circumstances and the combination of traits

possessed by immigrants and residents (e.g. Grant &

Grant 2008).

In the beetle genus Galapaganus, diversiﬁcation was

within island on San Cristobal, one of the oldest

islands, and within-island speciation could not be

rejected for the Santa Cruz clade; in both cases, shifts

to highland habitats seem to have evolved indepen-

dently (Sequeira et al. 2008). Although this habitat shift

is consistent with selection contributing to within-

island diversiﬁcation, it is not known whether it is

associated with a corresponding adaptive shift in

phenotype. Notably, Sequeira et al. (2008) inferred

that speciation did not occur within the younger island

of Isabela, where diversity is the result of between-island

colonization. Similarly, Parent & Crespi (2006) found a

combination of within- and between-island speciation in

Gala

pagos bulimulid snails. Polyphyletic land snail

assemblages were found on islands centrally located in

space and time (Isabela, Santa Cruz, Pinzo

n, Santiago),

whereas the more isolated islands of Espan

ola, San

Cristobal and Floreana (again in both space and time)

were occupied mostly by monophyletic assemblages

resulting from within-island diversiﬁcation. Some buli-

mulid species occur in sympatry and may have adapted to

the different habitats where they occur (Coppois &

Glowacki 1983; C. E. Parent & B. J. Crespi 2000–2005,

unpublished data). However, the relative importance

of drift and selection in within-island diversiﬁcation of

this group is not known.

The beetle genus Stomion has also diversiﬁed both

within and between islands ( Finston & Peck 2004).

Each population contains only one morphospecies,

and even on large islands such as Santa Cruz and

Isabela where two or three species occur, they never

occur in sympatry. Finston & Peck (2004) therefore

suggested that speciation happened in allopatry.

Stomion species have low vagility, even at very small

local scales ( Finston et al. 1997), which should

promote micro-allopatric speciation, in agreement

with the scenario proposed by Finston & Peck

(2004). No evidence of ecological or morphological

adaptation has been found in the genus (Finston &

Peck 1997, 2004), strengthening the idea that diversi-

ﬁcation happens via micro-allopatric speciation within

islands following between-island colonization. Peck

(1990) has suggested that troglobites (cave-dwelling

invertebrates) might provide good examples of diversi-

ﬁcation within islands. There are several examples of a

cave-dwelling form that has a sister species living

nearby outside the cave (Peck 1990; Peck & Finston

1993), but without a molecular phylogeny we cannot

tell how these species were formed.

In sum, the clearest cases of within-island speciation

occur in taxa with low vagility and on large islands with

diverse habitats. Isabela, with several volcanoes separ-

ated by recent lava ﬂows, is especially conducive to

within-island diversiﬁcation. In some cases, subsets of

taxa have found their way to other islands, making it

more difﬁcult to distinguish within-island speciation

from multiple between-island speciation events. For

more vagile taxa, speciation between islands seems

more likely, given the extreme habitat differences

among islands; but within-island processes are often

difﬁcult to rule out, and in either case, ecological

specialization can play an important role.

3356 C. E. Parent et al. Review. Diversiﬁcation of Gala

pagos terrestrial fauna

Phil. Trans. R. Soc. B (2008)

The number of species on an island depends on

speciation, colonization and extinction rates. The

three processes are affected by biogeography (island

area, elevation and insularity) and ecology (habitat

diversity). However, the species diversity equilibrium is

dynamic and changes through time because islands

themselves change (Whittaker et al. 2008). Moreover,

a delay is expected between the time an island becomes

available for colonization and speciation, and the time

equilibrium is reached. For example, Parent & Crespi

(2006) found that the younger islands of Fernandina

and Isabela had fewer land snail species than expected

based on their area, elevation and insularity. Similarly,

there are only two species of ﬂightless Galapaganus

beetles on Isabela, whereas San Cristobal, Santa Cruz

and Floreana each has three species (Sequeira et al.

2008). By contrast, there are more species of the moth

genus Galagete on Isabela and Fernandina (eight each)

than on any of the older islands (Schmitz et al. 2007).

This contrast among lineages might be a reﬂection of

their different dispersal capacity or the stochasticity of

interisland dispersal in some lineages.

Furthermore, the geographical conﬁguration of the

whole archipelago is dynamic, and there have been

changes in island number, size and isolation due to sea-

level variation on various time scales. On a short time

scale (from now back to the Pleistocene), it appears

that changes in sea levels created terrestrial avenues for

gene ﬂow during glacial periods that disappeared when

sea levels rose. The effect this sea level change can have

on species diversity on Gala

pagos has been relatively

unexplored, but Jordan & Snell (2008) suggested that

lava lizard diversity might have increased if islands

had been isolated for longer periods. Environmental

changes over the short term can inﬂuence the

evolutionary trajectory of species (Grant 1999), so it

is also likely that longer term climate changes have had

an important effect on the evolution and extinction of

species that remains largely unknown. A sobering

example comes from a recent study on El Nino effects

on levels of genetic diversity in Gala

pagos marine

iguanas (Steinfartz et al. 2007), in which even species

with large population sizes may suffer dramatic

collapses in genetic diversity when populations are

subject to frequent and possibly recurrent environ-

mentally devastating events.

6. FUTURE PROSPECTS FOR EVOLUTIONAR Y

RESEARCH ON GALA

PAGOS ISLANDS

Despite the large volume of evolutionary research that

has been undertaken in Gala

pagos, several species

groups remain relatively unstudied in terms of diversi-

ﬁcation within Gala

pagos and their relationship to

possible sources of colonists (table 2). Most phyloge-

netic studies of Gala

pagos organisms have been based

on mtDNA, sometimes in combination with one or a

few nuclear markers. Mitochondrial DNA has desir-

able properties for phylogenetic inference (Avise

2000), but the likelihood that a single locus reﬂects

the history of species and populations decreases when

divergence occurs rapidly and recently (Hudson &

Coyne 2002), as for much of the diversiﬁcation in the

Gala

pagos. Multilocus studies of sequence variation,

such as intron locus variation (Edwards et al. 2007),

offers some promise for providing more robust

estimates of phylogenetic and phylogeographic diver-

gence. However, in the only case in which they have

been used, giant tortoises, they were not helpful

(Caccone et al. 2004). For more vagile taxa such as

winged insects and birds, multilocus microsatellites

now offer a powerful means to estimate even low levels

of gene ﬂow, admixture and population divergence.

Ecology and habitat specialization can be critical

factors in speciation both within and between islands.

Phylogenetic studies can be broad but are limited in their

ability to reveal speciation processes. The number of

studies of natural history, ecology, evolution and

behaviour is small and limited in scope. Field studies

are limited spatially and temporally by logistics and

funding. Thus a great deal remains to be revealed about

speciation in Gala

pagos animals. One need only consider

a single ﬁeld research programme (Grant 1999; Grant &

Grant 2008) to see the magnitude of contributions to

the study of evolution and speciation that are possible.

7. CONSERVATION AND THE ROLE

OF EVOLUTIONARY GENETICS IN

GALA

PAGOS RESEARCH

While providing ecologists and evolutionary biologists

with ‘natural laboratories’, island biotas are also very

often in danger of going extinct. This is due both to

their generally small population sizes associated with

small geographical ranges, as well as to the relatively

simple ecosystems they inhabit (which is why they

are so valued by biologists). Island ecosystems are

therefore particularly susceptible to catastrophic

disturbances by invasive species. Understanding the

phylogenetics and biogeography of island species

allows greater insights into setting conservation

priorities and enacting rational conservation policies,

as illustrated in the examples below on Gala

pagos

tortoises (Powell & Caccone 2008).

Phylogenetic analysis detected previously unrecog-

nized taxa that deserve special conservation attention

(Russello et al. 2005) and assigned individuals of

unknown origin (zoo animals) to their correct location

(Burns et al. 2003; Russello et al. 2007b). Such studies

also allowed identiﬁcation of genetic lineages in

natural populations that were previously thought to

be extinct or nearly extinct (Russello et al. 2007a;

Poulakakis et al. 2005–2008, unpublished data).

Understanding the genetics of endangered island

biota may also aid in designing more rational recovery

efforts such as captive breeding/repatriation pro-

grammes (Milinkovitch et al. 2004, 2007).

Over the last century, the human population of

Gala

pagos has risen dramatically. Prior to 1900, fewer

than 300 people lived in the islands (Lundh 2001).

There are now nearly 30 000 residents on four

inhabited islands and more than 130 000 visitors

each year ( Watkins & Cruz 2007). The human

population boom has caused a marked increase in

introduced species and diseases (Fessl & Tebbich

2002; Wikelski et al. 2004; Gottdenker et al. 2005).

Several populations of birds have recently become

Review. Diversiﬁcation of Gala

pagos terrestrial fauna C. E. Parent et al. 3357

Phil. Trans. R. Soc. B (2008)

extinct (Grant 1999; Grant et al. 2005) and several

species are now threatened or on the brink of

extinction (e.g. Dvorak et al. 2004).

The near future will determine whether the

Gala

pagos will provide a model for the deterioration

of an island fauna in our time, or whether the brighter

prospect of effective management and persistence will

be realized so that future generations can continue to

study the processes of evolution in action.

We thank the staff of the Charles Darwin Research Station

and Parque Nacional de Gala

pagos for their continued

support and collaboration, and all the volunteers and

undergraduate and graduate students who have collaborated

in ﬁeld and laboratory work. We are grateful to E. Benavides,

F. Breden, B. Emerson, D. Geist, G. Gentile, S. Glaberman,

A. Hendry, M. A. Jordan, L. F. Keller, J. R. Powell,

P. Schmitz, A. Sequeira, F. Sulloway and S. Steinfartz, and

an anonymous reviewer for providing comments and for

sending unpublished results. We thank Michael Russello for

providing ﬁgure 1b. We also thank R. H. Cowie and S. A.

Trewick for their helpful comments and for giving us the

opportunity to contribute this review. A.C.’s work was

supported by NSF (DEB 322672 to J. R. Powell), YIBS-

Ecosave, the National Geographic Society, the Paul and Bay

Foundation and the AWARE Foundation; C.E.P.’s work was

supported by le Fonds Nature et Technologies du Que

bec

(FCAR), the Natural Sciences and Engineering Research

Council of Canada, Unitas Malacologica and the Conchol-

ogists of America; K.P.’s work was supported by NSF

(DEB 0317687).

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