Colonization and diversification: towards a phylogeographic synthesis for the Canary Islands
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REVIEWS
Colonization and diversification:
towards a phylogeographic synthesis
for the Canary Islands
Carlos Juan, Brent C. Emerson, Pedro Oromí and Godfrey M. Hewitt
Biogeography and ecology
T
he Canary Islands are his- Recently, the Canary Islands have become
torically and biologically a focus for studies of the colonization and The Canary Islands have a sub-
of particular interest. Pliny the diversification of different organisms. tropical climate; temperatures
the Elder heard about ‘Canaria, Some authors have considered Canarian are warm and show little seasonal
so called from the multitude of endemisms as relicts of Tertiary origin, variation. The climate is strongly
dogs (canes) of great size’, but new molecular data suggest a general influenced by the humid trade
through an expedition (c. 40 BC) pattern of continental dispersion followed by winds from the northeast, which,
to the islands by Juba II, King in situ speciation. Recent phylogeographic in combination with the altitude of
of Mauritania. The island of studies are revealing variants of the simple the volcanoes and the drier north-
El Hierro was chosen by Ptolemy stepping-stone colonization model that west winds blowing at higher lev-
as the prime meridian of longi- seems to hold for many Hawaiian groups. els, produce an inversion zone
tude because it was the most Many factors can generate deviations and marked vegetational zones
westerly place known in his from such a pattern: the stochastic (Box 2). Some of the most pecu-
time. The aboriginal inhabitants nature of colonization, competitive liar and interesting habitats in the
of the Canary Islands were the exclusion, phylogenetic constraints on Canary Islands are those pro-
Guanches, probably of Berber adaptive evolution and extinction. duced by the volcanic terrains,
origin1,2, who were conquered by An understanding of island colonization which are inhabited by special-
the Spanish in the 15th century. and diversification can best be developed ized animals9 (Box 3).
Following this, the Canaries be- from an ecosystem level synthesis as The Canarian fauna and flora,
came an important base for sea more data for the Canarian archipelago which is related to that of Madeira
journeys to the Americas and come to hand. and, to some extent, to that of the
Christopher Columbus replen- Azores and the Cape Verde Is-
ished all four of his westbound lands, has affinities with the Medi-
fleets at the islands. Carlos Juan is at the Departamento de Biologia, terranean region, although some
Universitat de les Illes Balears, elements are related to more re-
07071 Palma de Mallorca, Spain
The Canary archipelago (dbacjc8@clust.uib.es);
mote regions [Ceropegia (Asclepi-
The Canary Islands are situated in Brent Emerson and Godfrey Hewitt are at the adaceae) and Sideroxylon (Sapo-
the northeast Atlantic ocean be- School of Biological Sciences, taceae) to East Africa; Apollonias
tween 278379 and 298259N, and University of East Anglia, Norwich, UK NR4 7TJ (Lauraceae) to India; Bystropogon
138209 and 188109W (Box 1). The (b.emerson@uea.ac.uk, g.hewitt@uea.ac.uk); and (Lamiaceae) to South America;
nearest island (Fuerteventura) to Pedro Oromí is at the Departamento de Biología Picconia (Oleaceae) to Australia;
the continent lies approximately Animal, Facultad de Biología, Universidad de La Laguna, Vanessa indica (Nymphalidae) and
110 km off the northwest African 38205 La Laguna, Tenerife, Cyclyrius webbianus (Lycaenidae)
mainland (Cape Juby) and the Spain (poromi@ull.es). to Asia; Danaus spp. (Nymphali-
most distant island (La Palma) dae) to America and Ethiopian
lies 460 km off the mainland. The Africa, etc.]. Given the prevailing
archipelago has seven islets, and winds and the sea currents, two
seven main islands aligned from east to west: Lanzarote, plausible sources of colonizers are neighbouring North
Fuerteventura, Gran Canaria, Tenerife, La Gomera, La Palma Africa and the Iberian Peninsula. Endemism is high in the
and El Hierro. archipelago: about 27% of the approximately 1000 native
All the islands were formed in the past 20 million years vascular plant species and 50% of the terrestrial inverte-
(Ma) by volcanic eruptions. The central and western brate fauna (c. 6500 species) are endemic. Amphibians were
islands exceed 1400 m at the highest volcanoes, with Teide absent from the original fauna; only one snake has been
on Tenerife rising to 3718 m. The geological history of the recorded (already extinct), and apart from bats only five
islands is well documented3–6 (Box 1), providing a known mammals were present – two shrews and three rodents
temporal sequence for the origin of the islands and thus for (although rodents are now extinct).
their availability for colonization by diverse biota. The Some notable invertebrate families that occur on the
Pacific Hawaiian Islands and the Atlantic Canaries have mainland are absent, for example, from the order Coleop-
similarities, but also have distinctive differences, with the tera (Lucanidae, Geotrupidae and Lampyridae) and from
Atlantic Canaries having longer life, more complex vol- the order Hemiptera (Cicadidae, Naucoridae and Nepidae).
canic evolution and close proximity to the continent. In some instances complete orders are absent, such as the
Island formation is controversial; the two main competing Plecoptera and Phasmoptera. Other orders were originally
theories being a ‘hot spot’ origin and ‘propagating fracture’ absent but have been introduced, such as Scorpiones,
from the Atlas mountains7,8 (Box 1). Symphyla and Embioptera.
104 0169-5347/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(99)01776-0 TREE vol. 15, no. 3 March 2000REVIEWS
Examples of diversifi-
cation within the archipelago Box 1. Volcanism and the age of the islands
can also be found among The Canary archipelago originated from volcanic activity that began during the Oligocene [24.6–38 million years
vertebrates, notably geckos (Ma)]; the islands began to emerge during the past 21 Ma (Ref. 5).
(Tarentola), lizards (Gallotia)
and skinks (Chalcides). Incipi-
ent speciation processes (sub- Lanzarote (15.5)
species divergence) are oc- La Palma (2)
curring in some birds, such
as finches (Fringilla coelebs) Tenerife (11.6)
and blue tits (Parus caeruleus).
But, by far the most striking
cases of diversification are Gran Canaria (14–16)
among invertebrates, because La Gomera (10)
of either geographic isolation
or adaptation to diverse Fuerteventura (20)
niches. Some of the groups El Hierro (1)
(number of endemic species
in parenthesis) are: Gastro- Trends in Ecology & Evolution
poda10 – Napaeus (50) and
(Online: Fig. I)
Hemicycla (35); Araneae11
(M.A. Arnedo, PhD thesis, The ages of subaerial shields (shown in parentheses) decrease from east to west from 20 Ma for Fuerteventura
Universitat de Barcelona, to less than 1 Ma for El Hierro. Scale bar 5 100 km. It has been proposed that the archipelago is due to a mantle
1998) – Spermophorides (22), plume or hot spot with a slow plate motion, giving the longer life of Atlantic volcanoes compared with the Pacific
ones8. An alternative explanation relates the island formation to a fracture propagating from the Atlas mountains
Dysdera (44) and Oecobius with irregular velocity7. Another less supported theory is that of the uplifted blocks, based on the presence of
(34); Isopoda – Porcellio (18); mixed plutonic rocks and pillow lavas at as much as 1000 m above sea level6. Several periods of volcanic activ-
Diplopoda12 – Dolichoiulus ity and quiescence have occurred in the past 20 Ma on each island, with the exception of La Gomera4 – the only
(46); Collembola13 – Pholso- island in the archipelago without major activity for the past 4 Ma (although the last residual activity could be as
mides (16); Hemiptera14 – recent as 2 Ma).
Cyphopterum (24) and Erythro-
neura (23); Coleoptera15,16 –
Calathus (24), Cardiophorus (31), Attalus (51), Tarphius (30),
Hegeter (23), Nesotes (20), Laparocerus (66) and Acalles (18). Box 2. Vegetational zones
The central (Gran Canaria and Tenerife) and western (La Gomera, La Palma
Colonization pathways and the stepping-stone and El Hierro) islands have high volcanoes that for most of the year have
model cloud banks at around 1000 m on the windward slopes. These clouds are
DNA data are better suited for a phylogenetic tree than caused by the upper hot dry air and by the lower humid trade winds. As a
result, five vegetation zones can be distinguished: (1) arid subtropical scrub
morphology when interpreted in terms of dispersal (i.e. up to 250 m; (2) humid and semi-arid subtropical scrub, and woods from
colonization sequence)17. A morphological phylogenetic 250 to 600 m altitude; (3) humid laurel forest in the cloud belt from
tree is constrained by the ecogenetic adaptation to current 600–1000 m; (4) humid to dry temperate pine forest from 1000–2000 m;
and to recent selective pressures, but these are unlikely to and (5) dry subalpine scrub over 2000 m.
confound a DNA-based phylogeny. Recently, molecular
phylogenies have been obtained for Canarian lizards17–22, 3700
skinks23, geckos24, beetles25–31, butterflies32, Drosophila33,34,
cockroaches (I. Izquierdo, PhD thesis, Universidad de La
Laguna, Tenerife, 1997), bees35–37, spiders (M.A. Arnedo, PhD SW NE
thesis)38, mites39 and plants40–47. Most of these studies have Subalpine
made use of mitochondrial or chloroplast DNA sequences scrub
as a marker for inferring dispersal events between islands. 2200
In some of these taxa, the predominant pattern is similar to 2000
the one found for Hawaiian organisms; a stepwise coloniz- Pine
forest Cloud layer
ation sequence from older to younger islands in the chain.
1200
However, this simple pattern can be complicated by several 1100
Laurel forest
factors. Back colonization, recent colonization, within-island
differentiation, adaptation and extinction are some of the 600 Semiarid to humid woods 600 Trade
winds
historical events that confound a simple ‘island colonized Arid to semiarid scrub
300
as it emerges’ pattern.
Thorpe et al.17 have proposed two ways of interpreting a Trends in Ecology & Evolution
tree in terms of colonization sequence, taking into account
(Online: Fig. I)
biogeographical and genetic data. One method uses tree
topology and geography, based on the increased probability The eastern islands are influenced less by trade winds because of their
lower altitude and because rainfall is also scarcer owing to their geographic
of an island being colonized by founders from a closer island situation. An arid scrub with many xerophilous African plants dominates
than from a distant one. The other method of determining almost everywhere. Only on the top of a few mountains (Jandia in
the polarity of dispersal uses tree topology plus branch Fuerteventura and Famara in Lanzarote) can local hygrophilous endemisms
length. This method relies on the proposal that there is an be found. These are most probably the remains of more humid woods
occurring before the glaciations.
acceleration of divergence caused by a founder effect, thus
allowing discrimination between colonist and ancestor.
TREE vol. 15, no. 3 March 2000 105REVIEWS
model. Recent studies of Calathus31, a genus of ground
Box 3. Lava flow and lava-tube habitat beetles, have also revealed a phylogeographic pattern
The recent, barren lava flows are inhabited by ‘lavicolous’ species, which that conflicts with a stepping-stone colonization model.
are adapted to extreme conditions (drought, exposure to sun, temperature Calathus has colonized the Canary Islands at least twice
changes and no primary production)9. They feed on biological fall-out and and probably three times (mtDNA COI and COII sequence
are quickly replaced by competitors as soon as primary succession pro- data). The most recent colonization from the mainland
vides the lava with soil and plants (a few hundred years). The underground
environment is also peculiar in volcanic, oceanic islands, where basaltic
has occurred on the oldest islands of Fuerteventura and
flows prevail. The existing caves are lava tubes with the typical environ- Lanzarote.
mental conditions of caves (humidity, darkness and scarce food), but are
highly different in other features49. Unlike karstic caves, lava tubes are shal- Within-island phylogeography and volcanism
low, with roots inside, little running water and few ponds. The formation is Once an island has been colonized, within island differ-
quick and succession usually takes place upwards instead of downwards,
with troglobites moving closer to the surface as the lava ages and shallow entiation is facilitated by vicariance events produced by
passages become more isolated from the surface climate. This contrasts lava flows and by local extinctions followed by recolo-
with karstic caves where hypogean communities tend to extend deeper nization. This has been documented in many Hawaiian
down as time goes by. Succession in lava flows and volcanic caves is biota48. Across the islands of Fuerteventura and Lanzarote,
closely related. The timespan during which a lava tube provides a suitable
environment for particular adapted life forms is longer than in lavas, but
subaerial volcanic activity has been almost continuous
much shorter than in karstic caves. Collapsing and silting limit the tube in the past 20–22 Ma (Ref. 5). The current top layers
duration from 20 000 to 500 000 years. However, troglobites in the Canary of the islands are the result of two distinct cycles, one
Islands are not really fugitive species because the lava tubes are not their ranging from 21 to 12 Ma, and another ranging from 6 Ma
only habitat, they also occur in the cracks and voids of the bedrock and to prehistoric and historic eruptions. This volcanic activ-
in the mesocavernous shallow stratum, in medium and old volcanic ter-
rains. The variety of underground habitats, geological history and under- ity has resulted in a SSW (oldest) to NNE (youngest) age
ground barriers has led to the evolution of a rich troglobitic fauna in most of gradient for the surface terrains of Fuerteventura and
the islands. Lanzarote. This geological age gradient is consistent with
the mitochondrial genealogy (mtDNA COI sequence data)
found for the endemic Hegeter politus (Coleoptera, Tene-
The phylogeographic hypothesis for the lizard of the brionidae)30. This can be explained by an ancestral popu-
western Canary Islands, Gallotia galloti17–22, based upon lation in the south, which colonized in a northerly direction
recent studies using different DNA markers, is compatible following the progressive northward cessation of volcanic
with the time of emergence and the sequence of island for- activity.
mation. Gallotia galloti appears to have dispersed from A repeated phylogeographic pattern is found in di-
Tenerife along two independent pathways: one from north verse organisms on the island of Tenerife. Gallotia lizards,
Tenerife to La Palma, and the other from south Tenerife Chalcides skinks, Pimelia, Calathus and Eutrichopus beetles,
to La Gomera and to El Hierro. The sister group relation- Steganecarus mites, Dysdera spiders and Loboptera cock-
ship of the western G. galloti lineage to either G. stehlini roaches all possess vicariant sister taxa affiliated with the
(Gran Canaria) or the eastern G. atlantica (Fuerteventura Anaga and Teno massifs. The level of divergence between
and Lanzarote) is less robust21,22. Also compatible with the these sister lineages varies considerably among the differ-
stepping-stone model are the darkling beetles of the gen- ent taxa and molecular markers used, but, in all cases, this
era Pimelia and Hegeter26–30. Both show colonization pat- pattern can be related to the disjunct volcanic evolution of
terns that are essentially compatible with a stepwise dis- the island3. The relatively recent volcanic activity (less
persal from older islands in the east to younger islands in than 2 Ma) producing the Pico Viejo and Teide eruptions,
the west. A back colonization probably occurred from generated massive lava flows that joined the previously
Tenerife to Gran Canaria for Pimelia. The phylogenetic separate massifs of Anaga in the northeast and Teno in
relationships of brimstone butterflies32 (genus Gonepteryx) the northwest. These geologically old massifs (.4.5 Ma)
point to a North African ancestry for the Canarian taxa have not been covered by recent lava flows (Box 4). The
(three species) and subsequent within-archipelago disper- present-day distributions and phylogeographies of many
sals from Tenerife to La Gomera and Tenerife to La Palma. organisms in Tenerife can be related to the recent connec-
The colonization of the archipelago by Drosophila subob- tion of the massifs. For example, the beetle Pimelia shows
scura is also consistent with a stepping-stone model of two distinct mtDNA and ITS (internal transcribed spacer)
directional east–west migration33,34. lineages associated with the west and the east of Tenerife,
The phylogeography of the endemic skinks of the genus which probably originated on Teno and Anaga, respectively,
Chalcides23 is only partially concordant with a stepping- and spread over the central regions after the connective
stone colonization. A relatively recent dispersal from La eruptions28.
Gomera to El Hierro is apparently the only colonization The Gran Canarian skink Chalcides sexlineatus shows
following the ages of emergence of the islands. More considerable within-island morphological variation that
ancient colonizations between La Gomera and Tenerife, is, in part, coincident with genetic differentiation23. Simi-
and between Gran Canaria and Tenerife or La Gomera can lar morphological and genetic differentiation is present
be deduced, but the relationship of those clades with the in Tarentola geckos from Gran Canaria24. These phylo-
Fuerteventuran Chalcides simonyi lineage or with the North geographic patterns are probably related to vicariance
African outgroups is unclear. caused by the last volcanic cycle on the island approxi-
For the genus Tarentola24 (Gekkonidae), mitochondrial mately 2.8 Ma. There is a distinct possibility of mass
12S and cytochrome b sequences indicate several inde- extinctions about 3.4–4.5 Ma on Gran Canaria caused by
pendent colonization events from the continent. The phy- the violent emission of volcanic agglomerates over a great
logeny shows higher genetic divergences compared with part of the island. This could explain some of the back
Gallotia and Chalcides. The greater age of the Tarentola and relatively recent colonizations of Gran Canaria shown
group could have involved more extinction followed by by the phylogeographies of Dysdera, Calathus, Tarphius
replacement, generating a contemporary phylogenetic pat- (B. Emerson, unpublished), and possibly Chalcides and
tern that is not consistent with a simple stepping-stone Tarentola species.
106 TREE vol. 15, no. 3 March 2000REVIEWS Radiations, habitat shifts and adaptations Oceanic islands show considerable habitat diversity, pro- Box 4. Volcanic evolution of Tenerife duced by topology and humidity gradients, which, com- Anaga bined with their isolation, produces lower competition and empty ecological niches. This provides a template for 5.8 Ma the evolution of species radiations. For example, the plant 370–650 ka genus Argyranthemum has radiated into virtually all habi- 170 ka tats of the Atlantic islands42–47. In the Canarian archipelago,
REVIEWS
its own characteristic fauna, general patterns among islands 13 Fjellberg, A. (1993) Revision of European and North African
are seldom apparent within individual genera. Stochastic- Folsomides Stach with special emphasis on the Canarian fauna
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habitats. This response would typically have depended on 1–97
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cal requirements) and the competitive presence of other island lizards in relation to geological history: mtDNA, RFLP,
species within that niche. The potential for both rapid mor- cytochrome B, cytochrome oxidase, 12S rRNA and nuclear RAPD
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Island lizards (Gallotia galloti): 4-base endonuclease restriction
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data from DNA studies now allow us to assess the process phylogeny of the Tenerife Lacertid elucidate both historical causes and
of diversification within genera. Continued efforts to obtain morphological adaptation. Syst. Biol. 45, 335–343
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Acknowledgements 22 Rando, J.C. et al. (1997) Phylogenetic relationships of the Canary
We wish to thank Pablo Oromí for producing the figure of Islands endemic lizard genus Gallotia inferred from mitochondrial
volcanic evolution on Tenerife. We are also grateful for DNA sequences: incorporation of a new subspecies. Mol. Phylog. Evol.
comments on this article by three anonymous referees. This 8, 114–116
work has been supported by NERC and EU grants (G.M.H.) 23 Brown, R.P. and Pestano, J. (1998) Phylogeography of skinks
and by the Spanish DGICYT PB 96/0090 (P.O.). (Chalcides) in the Canary Islands inferred from mitochondrial DNA
sequences. Mol. Ecol. 7, 1183–1191
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Recreating ancestral proteins
Belinda S.W. Chang and Michael J. Donoghue
M
olecular evolution leaves lysozyme should be evident in a
Tracing the history of molecular changes using
behind a trail of amino acid phylogenetic methods can provide powerful phylogeny of primate lysozyme
substitutions potentially insights into how and why molecules work thesequences, on the lineage leading
rich in information about mol- to colobine monkeys. By inferring
way they do. It is now possible to recreate
ecular function. Tracing changes and comparing ancestral lysozyme
inferred ancestral proteins in the laboratory
in protein structure along the sequences, Messier and Stewart1
and study the function of these molecules.
branches of a phylogenetic tree were able to demonstrate adap-
This provides a unique opportunity to study
can provide important insights the paths and the mechanisms of functionaltive change in this lineage. Specifi-
into molecular function, and the change during molecular evolution. cally, they estimated the numbers
role of selection in shaping the What insights have already emerged from of nonsynonymous (dN) and syn-
relationship between molecular such phylogenetic studies of protein onymous (dS) substitutions along
structure and function. Recreation evolution and function, what are the each branch using Li’s method2,
of inferred ancestral proteins impediments to progress and what are the and found a dN/dS ratio much
using gene synthesis and protein prospects for the future? greater than one in the lineage
expression methods, whose bio- leading to the colobine monkeys
chemical functions can then be (Fig. 1). This analysis also re-
directly measured in vitro, pro- Belinda S.W. Chang and Michael J. Donoghue are vealed a previously unsuspected
vides a powerful approach to this at the Dept of Organismic and Evolutionary Biology, episode of positive selection in
Harvard University Herbaria, 22 Divinity Avenue,
problem. Cambridge, MA 02138, USA
the ancestral hominoid lineage.
(chang24@oeb.harvard.edu; Subsequently, Yang3 devel-
Phylogenies, molecular mdonoghue@oeb.harvard.edu). oped a more rigorous statistical
function and natural selection approach to this problem, using
Phylogenies can be used in several a codon-based maximum likeli-
ways to infer the effects of natural hood model of evolution4 to de-
selection on molecular function. tect elevated dN/dS ratios along
Because directional selection is known to elevate the ratio lineages in a phylogeny. Yang’s method3 uses likelihood
of nonsynonymous to synonymous nucleotide substitu- ratio tests to compare the performance of different likeli-
tions, this ratio can be used as a tool to detect lineages in a hood models, and to determine if the dN/dS ratio for the lin-
molecular phylogeny along which selection has occurred. eage of interest is elevated compared with other lineages
Cows and langur monkeys convergently evolved foregut in the phylogeny. This approach avoids using reconstructed
fermentation as a mechanism to digest the large amounts ancestral states as if these were actual observations in the
of plant material in their diets; a key component of this calculations of nonsynonymous and synonymous substi-
involved the recruitment of the lysozyme enzyme to digest tution rates. When applied to the primate lysozyme data,
foregut bacteria. Selection for this specialized function of this method showed strong evidence for positive selection
TREE vol. 15, no. 3 March 2000 0169-5347/00/$ – see front matter © 2000 Elsevier Science Ltd. All rights reserved. PII: S0169-5347(99)01778-4 109You can also read
