Inferring developmental modularity from morphological integration: Analysis of individual variation and asymmetry in bumblebee wings

C. P. Klingenberg, Alexander Badyaev, S. M. Sowry, N. J. Beckwith

Research output: Contribution to journalArticle

169 Citations (Scopus)

Abstract

Organisms are built from distinct modules, which are internally coherent but flexible in their relationships among one another. We examined morphological variation within and between two candidate modules: the fore- and hindwings of bumblebees (Hymenoptera: Apidae: Bombus empatiens). We used the techniques of geometric morphometrics (Procrustes superimposition) to analyze the variation of landmark configurations in fore- and hindwings. Regression was used to correct for size-related shape variation (allometry). Principal component analysis revealed patterns of variation that were remarkably similar for individual variation and fluctuating asymmetry (FA). Because covariation of FA among parts must be due to direct transmission of the developmental perturbations causing FA, this agreement of patterns suggests that much of individual variation is also due to direct developmental interactions within each developing wing. Moreover, partial least squares analysis indicated that the patterns of shape covariation between fore- and hindwings were nearly the same as the patterns of within-wing variation. Shape covariation of FA was only found in bees that had been reared under elevated CO2 concentration but not in bees from the control treatment, suggesting that the mechanisms of developmental interactions between fore- and hindwings are related to gas exchange. We conclude that the fore- and hindwings are developmental modules that maintain internal coherence through direct developmental interactions and are connected to each other only by relatively few links that use the system of interactions within modules.

Original languageEnglish (US)
Pages (from-to)11-23
Number of pages13
JournalAmerican Naturalist
Volume157
Issue number1
DOIs
StatePublished - 2001
Externally publishedYes

Fingerprint

fluctuating asymmetry
individual variation
Bombus
asymmetry
Apoidea
bee
Apidae
allometry
gas exchange
least squares
principal component analysis
Hymenoptera
organisms
perturbation
analysis
methodology

Keywords

  • Allometry
  • Developmental modules
  • Fluctuating asymmetry
  • Geometric morphometrics
  • Morphological integration
  • Shape

ASJC Scopus subject areas

  • Ecology

Cite this

Inferring developmental modularity from morphological integration : Analysis of individual variation and asymmetry in bumblebee wings. / Klingenberg, C. P.; Badyaev, Alexander; Sowry, S. M.; Beckwith, N. J.

In: American Naturalist, Vol. 157, No. 1, 2001, p. 11-23.

Research output: Contribution to journalArticle

@article{d7b6f95a94ed4c67872ada4ec6cb700b,
title = "Inferring developmental modularity from morphological integration: Analysis of individual variation and asymmetry in bumblebee wings",
abstract = "Organisms are built from distinct modules, which are internally coherent but flexible in their relationships among one another. We examined morphological variation within and between two candidate modules: the fore- and hindwings of bumblebees (Hymenoptera: Apidae: Bombus empatiens). We used the techniques of geometric morphometrics (Procrustes superimposition) to analyze the variation of landmark configurations in fore- and hindwings. Regression was used to correct for size-related shape variation (allometry). Principal component analysis revealed patterns of variation that were remarkably similar for individual variation and fluctuating asymmetry (FA). Because covariation of FA among parts must be due to direct transmission of the developmental perturbations causing FA, this agreement of patterns suggests that much of individual variation is also due to direct developmental interactions within each developing wing. Moreover, partial least squares analysis indicated that the patterns of shape covariation between fore- and hindwings were nearly the same as the patterns of within-wing variation. Shape covariation of FA was only found in bees that had been reared under elevated CO2 concentration but not in bees from the control treatment, suggesting that the mechanisms of developmental interactions between fore- and hindwings are related to gas exchange. We conclude that the fore- and hindwings are developmental modules that maintain internal coherence through direct developmental interactions and are connected to each other only by relatively few links that use the system of interactions within modules.",
keywords = "Allometry, Developmental modules, Fluctuating asymmetry, Geometric morphometrics, Morphological integration, Shape",
author = "Klingenberg, {C. P.} and Alexander Badyaev and Sowry, {S. M.} and Beckwith, {N. J.}",
year = "2001",
doi = "10.1086/317002",
language = "English (US)",
volume = "157",
pages = "11--23",
journal = "American Naturalist",
issn = "0003-0147",
publisher = "University of Chicago",
number = "1",

}

TY - JOUR

T1 - Inferring developmental modularity from morphological integration

T2 - Analysis of individual variation and asymmetry in bumblebee wings

AU - Klingenberg, C. P.

AU - Badyaev, Alexander

AU - Sowry, S. M.

AU - Beckwith, N. J.

PY - 2001

Y1 - 2001

N2 - Organisms are built from distinct modules, which are internally coherent but flexible in their relationships among one another. We examined morphological variation within and between two candidate modules: the fore- and hindwings of bumblebees (Hymenoptera: Apidae: Bombus empatiens). We used the techniques of geometric morphometrics (Procrustes superimposition) to analyze the variation of landmark configurations in fore- and hindwings. Regression was used to correct for size-related shape variation (allometry). Principal component analysis revealed patterns of variation that were remarkably similar for individual variation and fluctuating asymmetry (FA). Because covariation of FA among parts must be due to direct transmission of the developmental perturbations causing FA, this agreement of patterns suggests that much of individual variation is also due to direct developmental interactions within each developing wing. Moreover, partial least squares analysis indicated that the patterns of shape covariation between fore- and hindwings were nearly the same as the patterns of within-wing variation. Shape covariation of FA was only found in bees that had been reared under elevated CO2 concentration but not in bees from the control treatment, suggesting that the mechanisms of developmental interactions between fore- and hindwings are related to gas exchange. We conclude that the fore- and hindwings are developmental modules that maintain internal coherence through direct developmental interactions and are connected to each other only by relatively few links that use the system of interactions within modules.

AB - Organisms are built from distinct modules, which are internally coherent but flexible in their relationships among one another. We examined morphological variation within and between two candidate modules: the fore- and hindwings of bumblebees (Hymenoptera: Apidae: Bombus empatiens). We used the techniques of geometric morphometrics (Procrustes superimposition) to analyze the variation of landmark configurations in fore- and hindwings. Regression was used to correct for size-related shape variation (allometry). Principal component analysis revealed patterns of variation that were remarkably similar for individual variation and fluctuating asymmetry (FA). Because covariation of FA among parts must be due to direct transmission of the developmental perturbations causing FA, this agreement of patterns suggests that much of individual variation is also due to direct developmental interactions within each developing wing. Moreover, partial least squares analysis indicated that the patterns of shape covariation between fore- and hindwings were nearly the same as the patterns of within-wing variation. Shape covariation of FA was only found in bees that had been reared under elevated CO2 concentration but not in bees from the control treatment, suggesting that the mechanisms of developmental interactions between fore- and hindwings are related to gas exchange. We conclude that the fore- and hindwings are developmental modules that maintain internal coherence through direct developmental interactions and are connected to each other only by relatively few links that use the system of interactions within modules.

KW - Allometry

KW - Developmental modules

KW - Fluctuating asymmetry

KW - Geometric morphometrics

KW - Morphological integration

KW - Shape

UR - http://www.scopus.com/inward/record.url?scp=0035128629&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0035128629&partnerID=8YFLogxK

U2 - 10.1086/317002

DO - 10.1086/317002

M3 - Article

C2 - 18707232

AN - SCOPUS:0035128629

VL - 157

SP - 11

EP - 23

JO - American Naturalist

JF - American Naturalist

SN - 0003-0147

IS - 1

ER -