Intraspecific heterochrony and life history evolution: Decoupling somatic and sexual development in a facultatively paedomorphic salamander

Ryan, Travis J.; Semlitsch, Raymond D.

doi:10.1073/pnas.95.10.5643

Cited by 73 publications

(105 citation statements)

References 33 publications

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“…These processes have been evidenced in di¡erent urodele species (Harris 1987;Kalezic et al 1996;Ryan & Semlitsch 1998); the present study shows that both processes can produce paedomorphosis in natural populations of the same species.…”

Section: Discussionmentioning

confidence: 81%

“…Moreover, on the basis of Semlitsch's experiments (1987), high densities found for population B could also explain the large decrease in proportion of paedomorphs. Ryan & Semlitsch (1998) hypothesized that salamanders that do not metamorphose may have more energy available for growth or sexual development. They demonstrated this point in an experimental framework in which ambystomatid paedomorphs matured earlier than metamorphs.…”

Section: Discussionmentioning

confidence: 99%

“…Moreover, facultative paedomorphosis has been proved reversible, as paedomorphic individuals can experience metamorphosis (Semlitsch 1987). Several authors consider that paedomorphosis is an alternative ontogenetic pathway that should increase ¢tness in variable habitats (Whiteman 1994;Ryan & Semlitsch 1998). Although the evolution of plasticity in amphibians has been documented , the determinants of each alternative remain poorly understood.…”

Section: Introductionmentioning

confidence: 99%

“…In an experimental framework, Harris (1987) could conclude neither on progenesis nor on neoteny as the metamorphs and paedomorphs living in syntopy under water reached maturity at the same age, whereas the metamorphs that lived on land matured later. In a laboratory study focusing on age at ¢rst reproduction in Ambystoma, Ryan & Semlitsch (1998) demonstrated earlier maturation in paedomorphs than in metamorphs, but without growth variation.…”

Section: Introductionmentioning

confidence: 99%

“…They di¡er in that ¢rst reproduction occurs in neotenic individuals at the same age as in metamorphosed individuals, whereas it occurs at an earlier age in progenetic individuals. The process by which sexual development is decoupled from somatic development is of particular interest (Ryan & Semlitsch 1998) because sexual maturation has been shown to respond to selective pressures (Ro¡ 1992;Stearns 1992). Neoteny and progenesis di¡er in their life history and ecological implications.…”

Section: Introductionmentioning

confidence: 99%

See 4 more Smart Citations

Neoteny and progenesis as two heterochronic processes involved in paedomorphosis inTriturus alpestris(Amphibia: Caudata)

Denoël

Joly

2000

Proc. R. Soc. Lond. B

115

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Current theories on the evolution of paedomorphosis suppose that several ontogenetic pathways have appeared according to di¡erent selective pressures. The aim of this study was to ¢nd out whether two distinct processes can lead to paedomorphosis in the Alpine newt, Triturus alpestris. In this respect, we compared age structures of paedomorphic and metamorphic individuals in two newt populations where the two forms lived syntopically. Whereas paedomorphosis resulted in a slower rate of somatic development in one population, it resulted in an acceleration of sexual maturation in the other population. These processes correspond to neoteny and progenesis, respectively. These results suggest that phenotypic plasticity can result from contrasted ontogenetic pathways between two populations of the same species. They give support to models that consider gonadic development as the target of selection under di¡erent environmental pressures.

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Section: Discussionmentioning

confidence: 81%

Section: Discussionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

See 3 more Smart Citations

Neoteny and progenesis as two heterochronic processes involved in paedomorphosis inTriturus alpestris(Amphibia: Caudata)

Denoël

Joly

2000

Proc. R. Soc. Lond. B

115

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Uncoupling of sequential heteromorphic developmental programs

Farkas

Wache

Jones

1999

Arch. Insect Biochem. Physiol.

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The regulatory basis for differences among species in the developmental rate at which successive life stages are reached (“heterochrony”) is a subject of much controversy among vertebrate and invertebrate developmental biologists. The heterochrony in development of different insect species is characterized in part by the intercalcation between the embryo and adult of a (varied) number of heteromorphic larval instars. These heteromorphic larval instars exhibit changes of body form from one larval instar to the next, prior to the final metamorphic molt to the pupal form. The intractability of larval heteromorphosis to experimental dissection is due in part to the lack of suitable experimental probes that can test the nature of the coupling of each heterochronically expressed instar‐specific program. The epistatic basis of expression of heteromorphic developmental programs was assessed by two‐dimensional electrophoretic analysis of hemolymph proteins during the normal and experimentally manipulated feeding stages of the 3rd, 4th, and 5th (final) instar larvae, and during the prepupal stage, of Trichoplusia ni. Of the several hundred protein spots tracked, some were identified that were uniquely detected during a single stage, while others were observed during combinations of certain stages. The nature of coupling of sequential heterochronic expression of these proteins during successive instars or stages was tested by use of a parasite (Chelonus sp.) That injects regulatory material into the host embryo that later causes the subsequent precocious expression of the final instar larval program. Following the expression of a normal 3rd instar pattern, such larvae were observed to omit expression of the 4th instar program, including omission of the proteins heteromorphically specific to that instar, and instead then express an essentially normal final instar pattern. Thus, normal expression of the final instar feeding stage pattern was not invariantly coupled to prior expression of the penultimate instar‐specific proteins or pattern. Also, expression of the full program of the final instar feeding stage was epistatic to the penultimate instar program, i.e., the protein pattern unique to the penultimate larval instar was not co‐expressed with the precociously expressed final instar pattern. Larvae developmentally redirected in this manner failed to fully express the final instar prepupal stage pattern of protein expression, due at least in part to failed expression of prepupal ecdysteroids, but this was shown not to arise from omission of any of the first 4 larval instars per se. The nature of the redirections in host development caused by this parasite finally provides means of probing the coupling of successive expression on heteromorphic programs during larval development. Arch. Insect Biochem. Physiol. 40:1–16, 1999. © 1999 Wiley‐Liss, Inc.

show abstract

Uncoupling of sequential heteromorphic developmental programs

Farkas

Wache

Jones

1999

Arch. Insect Biochem. Physiol.

View full text Add to dashboard Cite

The regulatory basis for differences among species in the developmental rate at which successive life stages are reached ("heterochrony") is a subject of much controversy among vertebrate and invertebrate developmental biologists. The heterochrony in development of different insect species is characterized in part by the intercalcation between the embryo and adult of a (varied) number of heteromorphic larval instars. These heteromorphic larval instars exhibit changes of body form from one larval instar to the next, prior to the final metamorphic molt to the pupal form. The intractability of larval heteromorphosis to experimental dissection is due in part to the lack of suitable experimental probes that can test the nature of the coupling of each heterochronically expressed instar-specific program. The epistatic basis of expression of heteromorphic developmental programs was assessed by two-dimensional electrophoretic analysis of hemolymph proteins during the normal and experimentally manipulated feeding stages of the 3rd, 4th, and 5th (final) instar larvae, and during the prepupal stage, of Trichoplusia ni. Of the several hundred protein spots tracked, some were identified that were uniquely detected during a single stage, while others were observed during combinations of certain stages. The nature of coupling of sequential heterochronic expression of these proteins during successive instars or stages was tested by use of a parasite (Chelonus sp.) that injects regulatory material into the host embryo that later causes the subsequent precocious expression of the final instar larval program. Following the expression of a normal 3rd instar pattern, such larvae were observed to omit expression of the 4th instar program, including omission of the proteins heteromorphically specific to that instar, and instead then express an essentially normal final instar pattern. Thus, normal expression of the final instar feeding stage pattern was not invariantly coupled to prior expression of the penultimate instar-specific proteins or pattern. Also, expression of the full program of the final instar feeding stage was epistatic to teh penultimate instar program, i.e., the protein pattern unique to the penultimate larval instar was not co-expressed with the precociously expressed final instar pattern. Larvae developmentally redirected in this manner failed to fully express the final instar prepupal stage pattern of protein expression, due at least in part to failed expression of prepupal ecdysteroids, but this was shown not to arise from omission of any of the first 4 larval instars per se. The nature of the redirections in host development caused by this parasite finally provides means of probing the coupling of successive expression on heteromorphic programs during larval development.

show abstract

Intraspecific heterochrony and life history evolution: Decoupling somatic and sexual development in a facultatively paedomorphic salamander

Cited by 73 publications

References 33 publications

Neoteny and progenesis as two heterochronic processes involved in paedomorphosis inTriturus alpestris(Amphibia: Caudata)

Neoteny and progenesis as two heterochronic processes involved in paedomorphosis inTriturus alpestris(Amphibia: Caudata)

Uncoupling of sequential heteromorphic developmental programs

Uncoupling of sequential heteromorphic developmental programs

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