Allometry: The Big Picture

Biological diversity is dominated by variation in shape. This is perhaps no more apparent than in one of the most successful metazoan taxa, the insects. From a very simple body plan (head, thorax, abdomen, a pair of antenna, two pairs of wings and three pairs of legs) comes myriad forms, from bees to beetles, and fleas to flies. Much of this diversity is a result of variation in the relative, rather than the absolute, size of the insect body parts. This variation can be illustrated as a plot of the relative size of two structures among members of a population of animals (Figure 1). This is called a static allometry. When we think about variation in shape, we are often thinking about variation in static allometry (even though we might not realize it!).

  Figure 1: Diversity of slopes and intercepts of static allometries among social aphids. Ellipses represent the allometric relationship between fore femur length and body size (red lines on inset image) for two aphids species (light and dark gray). The lines through the ellipses show the mean allometry for the worker caste (dashed line) and soldier caste (heavy line). Dashed gray line is isometry or a 1:1 scaling relationship.

 

Figure 1: Diversity of slopes and intercepts of static allometries among social aphids. Ellipses represent the allometric relationship between fore femur length and body size (red lines on inset image) for two aphids species (light and dark gray). The lines through the ellipses show the mean allometry for the worker caste (dashed line) and soldier caste (heavy line). Dashed gray line is isometry or a 1:1 scaling relationship.

Despite the evolutionary importance of allometric variation we know almost nothing about the developmental processes that regulate static allometry. Consequently, we have very little idea of the types of genes and developmental pathways that have evolved to generate variation in allometric relationships. The long term goal of our research is to understand the developmental mechanisms that control static allometry in animals and how it evolves.

Most of our current work focuses on understanding the different aspects of development that control static allometry, using the fruit fly Drosophila melanogaster as our model organism. We have also been interested in  how allometric variation among aphids affects their behavior and ecology. Below are some of the projects being conducted in our laboratory.

What controls male genital size (in flies!)?

One fascinating aspect of size regulation is that variation in body size within a species is not necessarily accompanied by similar variation in the size of individual organs. For example, among humans, smaller individuals tend to have correspondingly smaller arms and legs, lungs and livers. However, the same is not true for brain size. Brain size tends to be roughly constant across a range of body sizes in humans, a condition called hypoallometry. Consequently, smaller humans have proportionally larger brains (relative to body size) than larger humans.

  Figure 2: The relationship between brain and body size in humans. Dashed gray line is isometry or a 1:1 scaling relationship. Data from Koh et al. Neuroreport 16, 2029-32.

 

Figure 2: The relationship between brain and body size in humans. Dashed gray line is isometry or a 1:1 scaling relationship. Data from Koh et al. Neuroreport 16, 2029-32.

There are probably good reasons why brain size varies less than body size in humans - brains are important organs, and development has likely evolved to ensure that conditions that result in a reduction in adult size (for example malnutrition during childhood) retard the growth of the body more than the growth of the brain. However, we have no idea how this is achieved.

In fruit flies, it is not the brain that is hypoallometric to body size, but the male genitals. Consequently smaller male flies tend to have proportionally larger genitals than larger male flies. Over the past few years we have sought to understand the developmental mechanisms that regulate this phenomenon. Early work suggests that differences in the way the insulin-signaling pathway regulates the growth of the genitals compared to other organs is key. Thus the insulin-signaling pathway, which plays a major roles in longevity, diabetes, and the regulation of cell, organ and body size, may be centrally involved in regulating allometry.

Dreyer, A.P., Saleh Ziabari, O., Swanson, E.M., Chawla, A., Frankino, W.A., Shingleton, A.W. 2015. Cryptic individual scaling relationships and the evolution of morphological scalingIn review.

Stillwell, R.C., Shingleton, A.W, Dworkin, I., Frankino, W.A. 2015. Tipping the scales: Evolution of the allometric slope independent of average trait sizeIn revision.

Shingleton, A.W., Frankino, W.A. 2013. New perspectives on the evolution of exaggerated traits. BioEssay, 35, 100-107

Shingleton, A.W., Tang, H.Y. 2012. Plastic flies: The regulation and evolution of trait variability in Drosophila. Fly, 6, 1-3

Tang, H., Smith-Caldas, M.S.R., Driscoll, M.V., Salhadar, S. & Shingleton, A.W. 2011. FOXO regulates organ-specific phenotypic plasticity in DrosophilaPLoS Genetics, 7, e1002373

Dreyer, A.P., Shingleton, A.W. 2011. The effect of genetic and environmetal variation on genital size in male Drosophila: Canalized but developmentally unstable. PLoS One, 6, e28278

Shingleton, A.W., Estep, C.M., Driscoll, M.V., Dworkin, I. 2009. Many ways to be small: Different environmental regulators of size generate different scaling relationships in Drosophila melanogaster. Proceedings of the Royal Society, London. Series B, 276, 2625-2633

Frankino, W.A., Emlen, D.J. & Shingleton, A.W. 2009. Experimental approaches to studying the evolution of morphological allometries: The shape of things to come. in "Experimental Evolution(T. Garland & M.R. Rose, Eds), University of California Press, Berkley.

Shingleton, A.W., Mirth, C.K. & Bates, P.W. 2008Developmental model of static allometry in holometabolous insects. Proceedings of the Royal Society, London. Series B, 275, 1875-1885

Shingleton, A.W., Frankino, W.A., Flatt, T. Nijhout, H.F. & Emlen, D.J. 2007.Size and Shape: The regulation of static allometry in insects, BioEssays, 29 (6), 536-548

Shingleton, A.W., Das, J., Vinicius, L. & Stern, D.L. 2005. The temporal requirements for insulin signaling during development in Drosophila, PLoS Biology, 3 (9)

What Controls Body and Organ Size?

An important aspect of the control of allometry is the control of body size.  In holometabolous insects (insects that form pupae), final body size is regulated by the point in development when a larva decides to stop growing and begin to pupate. This decision is made when the larvae reaches a particular size, called the critical size. We are interested in how an insect knows when it has reached critical size. Early research suggested that damage to the developing organs in a fly (called imaginal discs) can delay development. This suggests that the imaginal discs may need to be at a certain size for a fly to reach critical size and initiate metamorphosis. We have been using various physical and genetic methods to alter the growth of imaginal discs and see how this affects critical size. Our data indicate that the imaginal discs do indeed help regulate critical size and the timing of metamorphosis. Even more excitingly, we have discovered that slowing the growth of one imaginal disc slows the growth of all other organs in the body. This suggests that body and organ size is controlled by a complex set of signals by which growing organs 'talk' to one another. On going work in the lab is directed to identifying the nature of these signals.

Herbosa, L., Oliviera, M.M., Talamillo, Pérez, C., González, M., Martín, D., Sutherland, J.D., Shingleton, A.W., Mirth, C.K., Barrio, R. 2015. Ecdysone promotes growth of imaginal discs through the regulation of Thor in D. melanogaster. Scientific Reports. online ahead of print.

Oliveira, M.M., Shingleton, A.W., Mirth, C.K. 2014. Tissue pattern is not tightly coordinated with whole body development. PLoS Genetics. 10(6): e1004408

Mirth, C.K., Tang, H., Makohon-Moore, S., Salhadar, S., Gokhale, R.H., Riddiford, L.M., Shingleton, A.W., 2014. Juvenile hormone regulates body size and perturbs insulin-signaling in Drosophila. Proceedings of the National Academy of Sciences, USA, doi: 10.1073/pnas.1313058111

Callier, V., Shingleton, A.W., Brent, C.S., Ghosh, S.M., Kim, J., Harrison, J.F., 2013. The role of reduced oxygen in the developmental physiology of growth and metamorphosis initiation in Drosophila melanogaster. The Journal of Experimental Biology, 216, 4334-4340.

Parker, N.F. & Shingleton, A.W. 2011. The coordination of growth among Drosophila organs in response to localized growth perturbation. Developmental Biology, 357, 318-325

 Shingleton, A.W. 2011. The regulation and evolution of growth and body size. in"Mechanisms of Life History Evolution" (T. Flatt & A. Heyland, Eds), OUP

Stieper, B.C., Kupershtok, M., Driscoll, M.V. & Shingleton, A.W. 2008. Imaginal disc growth regulates the timing of metamorphosis in Drosophila melanogaster. Developmental Biology321, 18-26

Shingleton, A.W. 2005, Body-Size Regulation: Combining Genetics and Physiology, Current Biology, 15 (20), R825-R827

The evolutionary implications of changes in allometry

Allometric variation clearly underlies much of the morphological diversity we see around us. Nevertheless, how does an animal's allometry affect its fitness, and how does this influence the evolution of its morphology? We have been exploring the selective pressures that change allometry and how allometric change influences fitness through mathematical modeling, experimental evolution, evolutionary analysis and phylogenetic. This work started on aphids and continues in Drosophila,

Dreyer, A.P., Saleh Ziabari, O., Swanson, E.M., Chawla, A., Frankino, W.A., Shingleton, A.W. 2015 Cryptic individual scaling relationships and the evolution of morphological scaling. In review.

Stillwell, R.C., Shingleton, A.W, Dworkin, I., Frankino, W.A. 2015Tipping the scales: Evolution of the allometric slope independent of average trait sizeIn revision.

Shingleton, A.W., Frankino, W.A. 2013. New perspectives on the evolution of exaggerated traits. BioEssay, 35, 100-107

Frankino, W.A., Emlen, D.J. & Shingleton, A.W. 2009. Experimental approaches to studying the evolution of morphological allometries: The shape of things to come. in "Experimental Evolution(T. Garland & M.R. Rose, Eds), University of California Press, Berkley.

Shingleton, A.W., Stern, D.L. & Foster, W.A. 2005. The origin of a mutualism: a morphological trait promoting the evolution of ant-aphid mutualisms, Evolution, 59 (4), 921-926

Shingleton A.W. & Stern, D.L. 2003. Molecular phylogenetic evidence for multiple gains or losses of ant mutualism within the aphid genus Chaitophorus. Molecular Phylogenetics and Evolution, 26, 26-35.

Shingleton, A.W. & Foster, W.A. 2001. Behaviour, morphology and the division of labour in two soldier-producing aphids. Animal Behaviour, 62, 671-67

Shingleton, A.W. & Foster, W. A. 2000. Ant tending influences soldier production in a social aphid. Proceedings of the Royal Society, London. Series B, 267, 1863-1868.