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A MOLECULAR PHYLOGENETIC ANALYSIS OF REPRODUCTIVE TRAIT EVOLUTION IN THE SOFT CORAL GENUS ALCYONIUM

The soft coral genus Alcyonium is among the most reproductively diverse invertebrate taxa known: The genus includes species that vary both in mode of reproduction (including broadcast spawners, internal brooders, and external brooders) and sexual expression (gonochores, hermaphrodites, and a unisexu... Full description

Journal Title: Evolution 2001-01, Vol.55 (1), p.54-67
Main Author: McFadden, Catherine S.
Other Authors: Donahue, Rachel , Hadland, Brandon K. , Weston, Rebecca
Format: Electronic Article Electronic Article
Language: English
Subjects:
Publisher: Oxford, UK: Blackwell Publishing Ltd
ID: ISSN: 0014-3820
Link: https://www.ncbi.nlm.nih.gov/pubmed/11263746
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title: A MOLECULAR PHYLOGENETIC ANALYSIS OF REPRODUCTIVE TRAIT EVOLUTION IN THE SOFT CORAL GENUS ALCYONIUM
format: Article
creator:
  • McFadden, Catherine S.
  • Donahue, Rachel
  • Hadland, Brandon K.
  • Weston, Rebecca
subjects:
  • Adaptation, Physiological
  • Alcyonium
  • Animal reproduction
  • Animals
  • Aquatic life
  • Biological taxonomies
  • Cnidaria - anatomy & histology
  • Cnidaria - genetics
  • Cnidaria - physiology
  • cnidarian
  • Coral reef biology
  • Corals
  • Disorders of Sex Development
  • DNA, Ribosomal - genetics
  • Ecological life histories
  • Eggs
  • Embryos
  • Evolution
  • Evolution, Molecular
  • Fertilization
  • Genetic aspects
  • Hermaphroditism
  • Incubation
  • internal transcribed spacer
  • Larvae
  • Larval development
  • life-history evolution
  • Marine invertebrates
  • Molecular biology
  • molecular systematics
  • Parthenogenesis
  • Phylogeny
  • Polymerase Chain Reaction
  • Population Dynamics
  • Reproduction
  • ribosomal DNA
  • Sequence Analysis, DNA
  • sexual expression
  • soft coral
  • Spawning
ispartof: Evolution, 2001-01, Vol.55 (1), p.54-67
description: The soft coral genus Alcyonium is among the most reproductively diverse invertebrate taxa known: The genus includes species that vary both in mode of reproduction (including broadcast spawners, internal brooders, and external brooders) and sexual expression (gonochores, hermaphrodites, and a unisexual parthenogen). Such diversity offers a unique opportunity to examine associations between reproductive and morphological traits in a phylogenetic context. We used an approximately 900-bp sequence of the nuclear ribosomal gene complex spanning the internal transcribed spacer (ITS) regions to construct a molecular phylogeny for 14 European and North American species of Alcyonium onto which we mapped the known distribution of reproductive and morphological traits. The phylogeny suggests that hermaphroditism or parthenogenesis has evolved independently at least twice in this genus, and always in internally brooding species. Broadcast spawning and external brooding only occur in species with large colony size, whereas all species with small colony size brood their larvae internally. Internal brooding and small size appear to be ancestral in this genus; if this is the case, an association between broadcast spawning and large colony size has evolved independently in at least two clades. This tendency of small adults to brood their larvae while large adults broadcast spawn them into the plankton has been observed in a variety of solitary invertebrate taxa, but to date has not been documented in any other colonial invertebrates. Moreoever, it has been suggested that organisms with a colonial growth form should not experience the allometric constraints on brood space that have been proposed to explain the association between adult size and mode of reproduction in solitary organisms. Unlike many other colonial groups, however, module (polyp) size is strongly correlated with colony size in Alcyonium, and constraints on brooding may be imposed by module, rather than colony, allometry. The very close genetic relationship (< 1% sequence divergence) and shared polymorphisms among A. digitatum (a large, gonochoric broadcast spawner), A. siderium, and A. sp. A (intermediate-sized and small hermaphroditic, internal brooders) suggest that evolutionary transitions between broadcast spawning and brooding and between gonochorism and hermaphroditism can occur easily and rapidly in this group.
language: eng
source:
identifier: ISSN: 0014-3820
fulltext: no_fulltext
issn:
  • 0014-3820
  • 1558-5646
url: Link


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titleA MOLECULAR PHYLOGENETIC ANALYSIS OF REPRODUCTIVE TRAIT EVOLUTION IN THE SOFT CORAL GENUS ALCYONIUM
creatorMcFadden, Catherine S. ; Donahue, Rachel ; Hadland, Brandon K. ; Weston, Rebecca
creatorcontribMcFadden, Catherine S. ; Donahue, Rachel ; Hadland, Brandon K. ; Weston, Rebecca
descriptionThe soft coral genus Alcyonium is among the most reproductively diverse invertebrate taxa known: The genus includes species that vary both in mode of reproduction (including broadcast spawners, internal brooders, and external brooders) and sexual expression (gonochores, hermaphrodites, and a unisexual parthenogen). Such diversity offers a unique opportunity to examine associations between reproductive and morphological traits in a phylogenetic context. We used an approximately 900-bp sequence of the nuclear ribosomal gene complex spanning the internal transcribed spacer (ITS) regions to construct a molecular phylogeny for 14 European and North American species of Alcyonium onto which we mapped the known distribution of reproductive and morphological traits. The phylogeny suggests that hermaphroditism or parthenogenesis has evolved independently at least twice in this genus, and always in internally brooding species. Broadcast spawning and external brooding only occur in species with large colony size, whereas all species with small colony size brood their larvae internally. Internal brooding and small size appear to be ancestral in this genus; if this is the case, an association between broadcast spawning and large colony size has evolved independently in at least two clades. This tendency of small adults to brood their larvae while large adults broadcast spawn them into the plankton has been observed in a variety of solitary invertebrate taxa, but to date has not been documented in any other colonial invertebrates. Moreoever, it has been suggested that organisms with a colonial growth form should not experience the allometric constraints on brood space that have been proposed to explain the association between adult size and mode of reproduction in solitary organisms. Unlike many other colonial groups, however, module (polyp) size is strongly correlated with colony size in Alcyonium, and constraints on brooding may be imposed by module, rather than colony, allometry. The very close genetic relationship (< 1% sequence divergence) and shared polymorphisms among A. digitatum (a large, gonochoric broadcast spawner), A. siderium, and A. sp. A (intermediate-sized and small hermaphroditic, internal brooders) suggest that evolutionary transitions between broadcast spawning and brooding and between gonochorism and hermaphroditism can occur easily and rapidly in this group.
editionReceived May 9, 2000. Accepted August 11, 2000.
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subjectAdaptation, Physiological ; Alcyonium ; Animal reproduction ; Animals ; Aquatic life ; Biological taxonomies ; Cnidaria - anatomy & histology ; Cnidaria - genetics ; Cnidaria - physiology ; cnidarian ; Coral reef biology ; Corals ; Disorders of Sex Development ; DNA, Ribosomal - genetics ; Ecological life histories ; Eggs ; Embryos ; Evolution ; Evolution, Molecular ; Fertilization ; Genetic aspects ; Hermaphroditism ; Incubation ; internal transcribed spacer ; Larvae ; Larval development ; life-history evolution ; Marine invertebrates ; Molecular biology ; molecular systematics ; Parthenogenesis ; Phylogeny ; Polymerase Chain Reaction ; Population Dynamics ; Reproduction ; ribosomal DNA ; Sequence Analysis, DNA ; sexual expression ; soft coral ; Spawning
ispartofEvolution, 2001-01, Vol.55 (1), p.54-67
rightsCopyright 2001 The Society for the Study of Evolution
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0A MOLECULAR PHYLOGENETIC ANALYSIS OF REPRODUCTIVE TRAIT EVOLUTION IN THE SOFT CORAL GENUS ALCYONIUM
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descriptionThe soft coral genus Alcyonium is among the most reproductively diverse invertebrate taxa known: The genus includes species that vary both in mode of reproduction (including broadcast spawners, internal brooders, and external brooders) and sexual expression (gonochores, hermaphrodites, and a unisexual parthenogen). Such diversity offers a unique opportunity to examine associations between reproductive and morphological traits in a phylogenetic context. We used an approximately 900-bp sequence of the nuclear ribosomal gene complex spanning the internal transcribed spacer (ITS) regions to construct a molecular phylogeny for 14 European and North American species of Alcyonium onto which we mapped the known distribution of reproductive and morphological traits. The phylogeny suggests that hermaphroditism or parthenogenesis has evolved independently at least twice in this genus, and always in internally brooding species. Broadcast spawning and external brooding only occur in species with large colony size, whereas all species with small colony size brood their larvae internally. Internal brooding and small size appear to be ancestral in this genus; if this is the case, an association between broadcast spawning and large colony size has evolved independently in at least two clades. This tendency of small adults to brood their larvae while large adults broadcast spawn them into the plankton has been observed in a variety of solitary invertebrate taxa, but to date has not been documented in any other colonial invertebrates. Moreoever, it has been suggested that organisms with a colonial growth form should not experience the allometric constraints on brood space that have been proposed to explain the association between adult size and mode of reproduction in solitary organisms. Unlike many other colonial groups, however, module (polyp) size is strongly correlated with colony size in Alcyonium, and constraints on brooding may be imposed by module, rather than colony, allometry. The very close genetic relationship (< 1% sequence divergence) and shared polymorphisms among A. digitatum (a large, gonochoric broadcast spawner), A. siderium, and A. sp. A (intermediate-sized and small hermaphroditic, internal brooders) suggest that evolutionary transitions between broadcast spawning and brooding and between gonochorism and hermaphroditism can occur easily and rapidly in this group.
subject
0Adaptation, Physiological
1Alcyonium
2Animal reproduction
3Animals
4Aquatic life
5Biological taxonomies
6Cnidaria - anatomy & histology
7Cnidaria - genetics
8Cnidaria - physiology
9cnidarian
10Coral reef biology
11Corals
12Disorders of Sex Development
13DNA, Ribosomal - genetics
14Ecological life histories
15Eggs
16Embryos
17Evolution
18Evolution, Molecular
19Fertilization
20Genetic aspects
21Hermaphroditism
22Incubation
23internal transcribed spacer
24Larvae
25Larval development
26life-history evolution
27Marine invertebrates
28Molecular biology
29molecular systematics
30Parthenogenesis
31Phylogeny
32Polymerase Chain Reaction
33Population Dynamics
34Reproduction
35ribosomal DNA
36Sequence Analysis, DNA
37sexual expression
38soft coral
39Spawning
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titleA MOLECULAR PHYLOGENETIC ANALYSIS OF REPRODUCTIVE TRAIT EVOLUTION IN THE SOFT CORAL GENUS ALCYONIUM
authorMcFadden, Catherine S. ; Donahue, Rachel ; Hadland, Brandon K. ; Weston, Rebecca
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1Alcyonium
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3Animals
4Aquatic life
5Biological taxonomies
6Cnidaria - anatomy & histology
7Cnidaria - genetics
8Cnidaria - physiology
9cnidarian
10Coral reef biology
11Corals
12Disorders of Sex Development
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14Ecological life histories
15Eggs
16Embryos
17Evolution
18Evolution, Molecular
19Fertilization
20Genetic aspects
21Hermaphroditism
22Incubation
23internal transcribed spacer
24Larvae
25Larval development
26life-history evolution
27Marine invertebrates
28Molecular biology
29molecular systematics
30Parthenogenesis
31Phylogeny
32Polymerase Chain Reaction
33Population Dynamics
34Reproduction
35ribosomal DNA
36Sequence Analysis, DNA
37sexual expression
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1Donahue, Rachel
2Hadland, Brandon K.
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atitleA MOLECULAR PHYLOGENETIC ANALYSIS OF REPRODUCTIVE TRAIT EVOLUTION IN THE SOFT CORAL GENUS ALCYONIUM
jtitleEvolution
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date2001-01
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volume55
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0University of Washington School of Medicine, Seattle, Washington 98195; E‐mail: rachelmd@u.washington.edu
11
2E‐l: Catherine_McFadden@hmc.edu
3Department of Medicine and Cell Biology, Washington University School of Medicine, St. Louis, Missouri 63110; E‐mail: hadlandb@msnotes.wustl.edu
abstractThe soft coral genus Alcyonium is among the most reproductively diverse invertebrate taxa known: The genus includes species that vary both in mode of reproduction (including broadcast spawners, internal brooders, and external brooders) and sexual expression (gonochores, hermaphrodites, and a unisexual parthenogen). Such diversity offers a unique opportunity to examine associations between reproductive and morphological traits in a phylogenetic context. We used an approximately 900-bp sequence of the nuclear ribosomal gene complex spanning the internal transcribed spacer (ITS) regions to construct a molecular phylogeny for 14 European and North American species of Alcyonium onto which we mapped the known distribution of reproductive and morphological traits. The phylogeny suggests that hermaphroditism or parthenogenesis has evolved independently at least twice in this genus, and always in internally brooding species. Broadcast spawning and external brooding only occur in species with large colony size, whereas all species with small colony size brood their larvae internally. Internal brooding and small size appear to be ancestral in this genus; if this is the case, an association between broadcast spawning and large colony size has evolved independently in at least two clades. This tendency of small adults to brood their larvae while large adults broadcast spawn them into the plankton has been observed in a variety of solitary invertebrate taxa, but to date has not been documented in any other colonial invertebrates. Moreoever, it has been suggested that organisms with a colonial growth form should not experience the allometric constraints on brood space that have been proposed to explain the association between adult size and mode of reproduction in solitary organisms. Unlike many other colonial groups, however, module (polyp) size is strongly correlated with colony size in Alcyonium, and constraints on brooding may be imposed by module, rather than colony, allometry. The very close genetic relationship (< 1% sequence divergence) and shared polymorphisms among A. digitatum (a large, gonochoric broadcast spawner), A. siderium, and A. sp. A (intermediate-sized and small hermaphroditic, internal brooders) suggest that evolutionary transitions between broadcast spawning and brooding and between gonochorism and hermaphroditism can occur easily and rapidly in this group.
copOxford, UK
pubBlackwell Publishing Ltd
pmid11263746
doi10.1111/j.0014-3820.2001.tb01272.x
tpages14
editionReceived May 9, 2000. Accepted August 11, 2000.