Adaptive Radiation

Secondary article Article Contents

Courtney J Murren, University of Tennessee, Knoxville, Tennessee, USA . Introduction

Adaptive radiation is a diversification of a single lineage into morphologically or physiologically distinct taxa that are adapted to a certain set of environmental conditions.

. Galapagos Finches . Hawaiian Fauna and Flora . South American Mammals

Introduction

. East African Great Lakes . Measuring Rates of Radiation

There is a large set of definitions of the term ‘adaptive radiation’ in the literature. Huxley, in 1942, defined adaptive radiation as ‘an invasion of different regions of the environment by different lines within a group and secondarily their exploitation of different modes of life’. Other definitions have focused on the concept of ecological niche (the set of environmental parameters that define the habitat of a particular species), such as Wilson (1992) ‘the spread of species with common ancestry into different niches’. Broadly, an adaptive radiation is a group of closely related species that have a character or set of characters that segregate these species, and that are adapted to the environments they occupy (Figure 1). There are two major evolutionary components considered to have led to adaptive radiations: (1) invasion of new environments and (2) release from competition. In many cases, both of these are important in speciation. (see Speciation: introduction.)

Taxon Species A Outgroup

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·········· Species B

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·········· Species C ·········· ·········· Species D ······ ·· Species E ····················

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Species F 2 Species G Species H Species I Species J

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Species K Figure 1 Schematic diagram of an adaptive radiation. The outgroup (species A) is the representative of an ancestral species that diverged prior to the diversification of the rest of the species (designated B–K). Three clades within a monophyletic group are considered (numbers 1–3) and are found in different environments. Dashed lines correspond to three different phenotypic characters that are found in all species within the group but not found in the other two groups. This unique character is an adaptation to the environment where that clade is found, which has allowed for the diversification within the clade.

Radiations have been frequently observed and studied on islands and other isolated habitats. These habitats have certain features in common: few organisms may colonize them, yet there may be several ecologically distinct zones. Radiations in these types of habitats are often thought to occur quickly over geological time. Exploitation of different habitats may have imposed differential selective pressures, resulting in divergence of species (Givnish and Sytsma, 1997). (see Islands.) Two organisms with identical ecological requirements will be the most severe competitors. The evolutionary corollary to competitive exclusion is that species that coexist will adapt to different habitats and resources. Selection may act to reduce competition among closely related species and allow for speciation (as observed in the Galapagos finches, Lack, 1947). This principle is particularly important when species are restricted to a specific geographic area (such as an oceanic island or an isolated lake). Coexisting species tend to diverge in their resource use to adapt to different environments. The release of competition simultaneously leads to the opening of ecological niches. A release from competition is considered as one possible hypothesis that led to the diversification of mammals following the extinction of the dinosaurs. (see Competition.) (see Vertebrate diversity and adaptation: overview.)

Empirical evidence The study of adaptive radiation requires the documentation of (1) the evolutionary relationships among the taxa and (2) the adaptive significance of the putatively adaptive character. The use of molecular approaches to construct a phylogeny has enabled recent advances into the study of adaptive radiations. Molecular markers serve as an independent data set to identify evolutionary relationships among taxa, upon which the phenotypic character of interest can be mapped. This alleviates problems where shared ecology without shared heritage influences the phenotypic expression of a particular trait. These molecular data are examined for monophyly (a group with a single ancestor). Genetic similarity among species within an adaptive radiation are often much greater than in other

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Adaptive Radiation

clades. Secondly, the demonstration that a character is adaptive can be examined through a variety of approaches. Comparisons of how traits function in different environments, experimental manipulations of phenotypes, and studies examining the link between fitness (survivorship or reproductive success) and phenotypes are three ways to identify the adaptive significance of a particular trait (for further discussion, see Reeve and Sherman, 1993 and Rose and Lauder, 1996). (see Molecular phylogeny reconstruction.) (see Gene expression - external and internal.) (see Fitness.)

Key innovation A ‘key innovation’ is the appearance of a novel character that corresponds with a transition to a new adaptive zone (e.g. nectar spurs of columbines; Hodges, 1997). Variation in this novel trait may facilitate the rapid divergence among species that exploit different environments or use resources in a new manner. In the columbine example (family Ranunculaceae: genus Aquilegia) a particular pollinator visits only nectar spurs of a certain length, thus the variation in this trait attracts different species of pollinator. Nectar spurs are considered a key innovation that allowed for specialization of different pollinators, which subsequently promoted speciation through reproductive isolation. Whether the diversification or the key innovation came first is a difficult question to answer. The question can be addressed, however, through experimental manipulations that examine how the novel character may influence speciation (e.g. through reproductive isolation) and through comparative studies across several groups that have similar characters. Key innovations are contrasted with selective pressures of a novel environment as a mechanism for, and occurring prior to, radiation (Hodges, 1997). (see Adaptation and natural selection: overview.) Adaptive radiations have been investigated for a wide array of taxa including the well-known examples of the Galapagos finches, Hawaiian fruitflies, Hawaiian honeycreepers, Hawaiian silverswords, fish from East African lakes and South American mammals.

Galapagos Finches Galapagos finches (Geospizidae) were made famous through the writings of Charles Darwin (Voyage of the Beagle, Darwin, 1845) and the detailed studies by Lack (1940, 1947). These birds are an especially good example of adaptive radiation that occurs in an island archipelago, where open habitats can be colonized followed by ecological specialization. The morphologies of the bills of Darwin’s finches are considered to be adaptations to a specific diet and eating behaviour. Species in the genus Geospiza are seed-eaters and include both the groundfinches, with thick heavy beaks, and the cactus-feeding 2

species, with conical beaks. The bills of these birds vary in sizes that reflect the size of seed that each species eats. Other genera include Platyspiza, which feed generally on buds and fruits; Camarhynchus, which are tree finches and primarily insect-eaters; Cactospiza, which use cactus spines to obtain arthropods as food; and Certidea, the warbler finches, which have a combined diet of nectar and insects. Lack observed that species with very similar beaks rarely occurred on the same island, and suggested that competition for food was an important selective pressure which allowed for morphological divergence (Lack, 1947). (see Darwin’s finches.) (see Darwin, Charles Robert.) Molecular data are consistent with the hypothesis that Darwin’s finches are derived from a single species and possibly a single founding event (Sato et al., 1999). The molecular data support the idea that the Cocos finch (Pinaroloxias) dispersed from the Galapagos relatively recently. The Cocos finch has a large genetic distance from the other tree finches, and this is possibly due to the ecologically distinct nature of Cocos Island. Grant and Grant (1996) examined the effect of the El Nin˜o on feeding patterns and mortality of three species of finches from the genus Geospiza. Their study showed that extreme environmental changes affect survival of both hybrid-species (hybrids have intermediate bill sizes from their parents) and two of the three species of Darwin’s finches, in association with decrease abundance of large seeds. Studies into the mechanisms behind the divergence and ecology of these species are ongoing (for further discussion see Grant, 1996).

Hawaiian Fauna and Flora The Hawaiian archipelago provides us with a unique example of evolution on islands, in part, because of its remarkable geology and history. The islands were formed in sequence from a volcanic hot spot, with the youngest of the present-day large islands (Hawaii, about 500 000 years old) in the south-east and the oldest (Kauai, about 5.3 million years old) in the north-west. The archipelago has the distinction of being the set of islands furthest away from any continent on the globe. Because of its geologic history and exceptionally large variation in elevation, Hawaii has a wide range of very different climatic regimes and a vast array of ecologically distinct habitats (Wagner and Funk, 1995). In some areas the rock is eroded into deep valleys separated by high ridges, leading to the isolation to populations over evolutionary time scales. These characteristics have contributed to the diversification of many groups of plants including the lobeliads and the silversword alliance and animals, including crickets, fruitflies, spiders, birds.

Adaptive Radiation

Hawaiian honeycreepers The isolation of the Hawaiian islands means that although they have been widely colonized by birds, yet few other terrestrial vertebrates have arrived from the continents. Historically, approximately 33 species of Hawaiian honeycreepers (Drepanidinae) were known from the Hawaiian islands (only 10 species are currently extant, and all are endangered). The Hawaiian honeycreepers are similar to the Galapagos finches in that they have a wide array of bill forms that reflect the feeding habits of the particular species. Recent studies using DNA to reconstruct the evolutionary relationships among species (a molecular phylogeny) are consistent with the biogeographic pattern shown in other Hawaiian organisms in which species divergence appears to have occurred following dispersal to younger islands (Tarr and Fleischer, 1995). (see Molecular phylogeny reconstruction.)

Hawaiian fruitflies Hawaiian fruitflies (Drosophilidae) are one of the most speciose examples of adaptive radiations known. It is thought that one or two initial founders led to the over 800 species of fruitflies currently known from Hawaii, making up 25% of the world’s diversity of drosophiloids. Among fruitflies, those from Hawaii have the greatest morphological, behavioural and ecological diversity on Earth. Endemism of a single island is extremely high, and is increased by certain species that have ranges restricted to a single patch of forest isolated by lava flows (a kipuka). Drosophila species differ in their male morphology, courtship patterns, and ecologically distinct breeding substrates. Despite these phenotypic differences, molecular analyses have supported the idea that Hawaiian fruitflies are a monophyletic group. Hawaiian drosophiloid diversification is a combined result of founding events on new islands or volcanoes, genetic drift, different selective pressures in the new environment, and sexual selection (DeSalle, 1995). (see Drosophila evolutionary genetics.)

province. In addition to founder events followed by speciation occurring on each successively younger island, ecological shifts appear to have occurred at least once on each island. Their habitats range in elevation from 75 m to 3750 m representing a dramatic gradient in rainfall. In particular, ecological shifts to bog habitats appear to have occurred several times throughout their history (Baldwin and Robichaux, 1995). Baldwin and Sanderson (1998) examined the age of the Hawaiian silversword alliance using DNA sequence data (internal transcribed spacer (ITS) region of nuclear ribosomal DNA) and a maximum likelihood statistical approach. These data suggest that the most recent common ancestor of the group to have colonized the islands arrived 5.2 (+ 0.8 SD) mya, which is close to the approximate age of the oldest current island, Kauai. (see Asterales (sunflower).) (see Plant biodiversity.)

South American Mammals Differentiation among the eutherian (placental) mammals occurred during the Palaeocene and the diversification of the modern orders occurred over approximately 10 million years. Tertiary mammals of South America, including armadillos, glyptodonts, anteaters, sloths, South American ungulates (e.g. Pyrotheria, Litopterna, Xenugulata lineage independent of the African ungulates) experienced adaptive radiations. Following the establishment of the Panamanian land bridge and by the end of the Pliocene many of these endemic species became extinct. Approximately half of the current South American fauna has ancestors that came from North America during the Pliocene. These North American migrants out-competed the resident mammal fauna. Although some species moved from south to north, these species were less successful, presumably as a result of their inferior competitive ability (Carroll, 1988). (see Eutheria (placental mammals).) (see Edentata and Pholidota (armadillos, anteaters and tree sloths).)

Hawaiian silverswords

East African Great Lakes

The Hawaiian silversword alliance includes three genera (Argyroxiphium, Wilkesia and Dubautia) of the sunflower family (Asteraceae). It is best known for the species of the genus Argyroxiphyium from which the name silversword was derived. This is a plant with silvery-hairy swordshaped leaves and a large showy flowering display. Growth forms of the alliance range from herbaceous mats and rosette plants, to trees, shrubs and lianas. Although these plants occur in a wide range of habitats (found on exposed lava to extremely wet forest) and have a range of growth forms, molecular data support this group as monophyletic. Morphological and molecular data suggest that the most recent common ancestor came from the California floral

The three great lakes of East Africa (Lake Victoria, Lake Tanganyika and Lake Malawi) were formed between 3 and 5 mya following geological activity that created rift valleys and mountains and led to the formation of large lake basins. One group of fish, the Cichlidae, have gone through an amazing radiation in these shallow lakes. Species differ morphologically, behaviourally and ecologically corresponding to their diet specialization. They range from algal scrapers, plankivores, insectivores, piscivores, paedophages and snail crushers, and some species are tremendously specialized to eat only fins, or scales of other fish. Variation in body shape and colour patterns are as dramatic as their trophic diversity. Their mating beha3

Adaptive Radiation

viour, polyandrous mating systems and leks also vary dramatically among species within a single lake. Most of the approximately 200 species found in Lake Victoria and the similar number in Lake Malawi are endemic to that lake. It is not clear whether feeding apparatus was a key innovation or whether sexual selection was responsible for reproductive isolation that was followed by morphological diversification. Recent DNA fingerprinting techniques have shown that for the rock-dwelling cichlids in Lake Malawi, closely related species were found to have similar jaw morphology, suggesting that trophic adaptation occurred prior to speciation events. However, further diversification (particularly evident in the male colour patterns) occurred within genera, suggesting that sexual selection may be an important influence in the adaptive radiation of at least some cichlid fishes (Albertson et al., 1999). In Lake Tanganyika, data from mtDNA (mitochondrial DNA) from cytochrome b suggest that fish with similar morphology are not necessarily part of a monophyletic lineage, and that there may have been multiple independent origins of these cichlids through divergence of species pairs (Ruber et al., 1999). Resource competition and selection for divergent resource-gaining morphologies is one possible explanation for the repeated and independent origin of similar phenotypes.

Measuring Rates of Radiation The pace of speciation and adaptive radiation can be measured through a variety of methods, including molecular clocks, using geological dates of island or lake formation, dating fossils or fossil pollen or a combination of these methods. For example, the Isthmus of Panama closed approximately 3 mya, creating a land bridge between North and South America. Meanwhile, the Caribbean and Pacific marine life became isolated. Using the geological date together with the mutation rate of a particular gene can generate a reasonable prediction on the time of speciation between the Caribbean and Pacific habitats. The amount of molecular divergence can be an indicator of whether the clade has recently radiated. Sequence divergence is expected to be low among species that have radiated recently in comparison with another group of closely related taxa. In contrast, species that have diverged earlier in history will have greater sequence divergence in comparison with closely related taxa (Givnish and Sytsma, 1997). (see Speciation and the fossil record.)

References Albertson RC, Markert JA, Danley PD and Kocher TD (1999) Phylogeny of a rapidly evolving clade: the cichlid fishes of Lake

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Malawi, East Africa. Proceedings of the National Academy of Sciences of the USA 96: 5107–5110. Baldwin BG and Sanderson MJ (1998) Age and rate of diversification of Hawaiian silversword alliance (Compositae). Proceedings of the National Academy of Sciences of the USA 95: 9402–9406. Baldwin BG and Robichaux RH (1995) Historical biogeography and ecology of the Hawaiian Silversword Alliance (Asteraceae): new molecular phylogenetic perspectives. In: Wagner WL and Funk VA (eds) Hawaiian Biogeography: Evolution on a Hot Spot Archipelago. Washington, DC: Smithsonian Institution Press. Carroll RL (1988) Vertebrate Paleontology and Evolution. New York: WH Freeman. Darwin C (1845) Journal of researches into the natural history and geology of the countries visited by the H.M.S. Beagle round the world, under the command of Capt. Fitz Roy, R.N., 2nd edn. London: John Murray. DeSalle R (1995) Molecular approaches to biogeographic analysis of Hawaiian Drosophilidae. In: Wagner WL and Funk VA (eds) Hawaiian Biogeography: Evolution on a Hot Spot Archipelago. Washington, DC: Smithsonian Institution Press. Grant BR and Grant PR (1996) High survival of Darwin’s finch hybrids: Effects of beak morphology and diets. Ecology 72: 500–509. Givnish TJ and Sytsma KJ (1997) Molecular Evolution and Adaptive Radiation. Cambridge: Cambridge University Press. Hodges SA (1997) Floral nectar spurs and diversification. International Journal of Plant Sciences 158: S81–S88. Huxley J (1942) Evolution: the Modern Synthesis. New York: Harper and Brothers. Lack D (1940) Evolution of the Galapagos finches. Nature 146: 324–327. Lack D (1947) Darwin’s Finches. Cambridge: Cambridge University Press. Reeve HK and Sherman PW (1993) Adaptation and the goals of evolutionary research. Quarterly Review of Biology 68: 1–32. Rose MR and Lauder GV (1996) Adaptation. New York: Academic Press. Ruber L, Verheyen E and Meyer A (1999) Replicated evolution of trophic specializations in an endemic cichlid fish lineage from Lake Tanganyika. Proceedings of the National Academy of Sciences of the USA 96: 10230–10235. Sato A, O’hUigin C, Figueroa F et al. (1999) Phylogeny of Darwin’s finches as revealed by mtDNA sequences. Proceedings of the National Academy of Sciences of the USA 96: 5101–5106. Tarr CL and Fleischer RC (1995) Evolutionary relationships of the Hawaiian Honeycreepers (Aves, Drepanidinae). In: Wagner WL and Funk VA (eds) Hawaiian Biogeography: Evolution on a Hot Spot Archipelago. Washington, DC: Smithsonian Institution Press. Wagner WL and Funk VA (1995) Hawaiian Biogeography: Evolution on a Hot Spot Archipelago. Washington, DC: Smithsonian Institution Press. Wilson EO (1992) The Diversity of Life. Cambridge, MA: Belknap Press.

Further Reading Futuyma DJ (1997) Evolutionary Biology. Sunderland, MA: Sinauer Associates. Grant PR (1986) Ecology and Evolution of Darwin’s Finches. Princeton, NJ: Princeton University Press. Lack D (1947) Darwin’s Finches. Cambridge: Cambridge University Press. Wagner WL and Funk VA (1995) Hawaiian Biogeography: Evolution on a Hot Spot Archipelago. Washington, DC: Smithsonian Institution Press.