Elsevier

Journal of Insect Physiology

Volume 44, Issue 11, November 1998, Pages 1081-1089
Journal of Insect Physiology

Body size and cell size in Drosophila: the developmental response to temperature

https://doi.org/10.1016/S0022-1910(98)00061-4Get rights and content

Abstract

In Drosophila, like most ectotherms, development at low temperature reduces growth rate but increases final adult size. Cultures were shifted from 25°C to low (16.5°C) or to high (29°C) temperature at regular intervals through larval and pupal stages, and the flies of both sexes showed an increase or decrease, respectively, in the size of thorax, wing and abdominal tergite. Size changes in the wing blade resulted from changes in the size of the epidermal cells (with only a small increase in cell number in males reared at low temperature). The temperature-shifts became less effective as they were made at successively later developmental stages, demonstrating a cumulative effect of temperature on adult size. The thorax and wing develop from the same imaginal disc, with most cell division occurring in larval stages, but they differ in timing of temperature sensitivity, which extends only to pupariation or into the late pupal stage, respectively. Growth of the adult abdomen occurs largely after pupariation but its size is temperature-sensitive through both larval and pupal stages. We discuss growth control in Drosophila and the likely effects of temperature on food assimilation, growth efficiency and allocation of nutrients to the production of different tissues.

Introduction

The size of an organism is a feature of great physiological and ecological importance (see Schmidt-Neilson, 1984, Peters, 1983). In most animals, a characteristic final body size is achieved by the control of growth through the embryonic and postembryonic phases of development, and the various body parts typically grow at different rates during different periods. Control of growth, although still poorly understood, is known to be closely integrated with the specification of patterns of cell differentiation within developing body parts (see Bryant and Simpson, 1984, Serrano and O'Farrell, 1997). Growth rate and final size may also be modulated by hormonal controls and may be constrained by many environmental factors, such as crowding or inadequate nutrition. Also, it has long been known that, in otherwise optimal conditions, a very wide range of ectotherms are characteristically influenced by their rearing temperature, with lower temperatures resulting in decreased growth rate, but an increase in final size reached at maturity (Ray, 1960, Atkinson, 1996von Bertalanffy, 1960).

In a comprehensive recent survey of the literature, Atkinson (1994), Atkinson (1996)demonstrated that this developmental effect of temperature on adult size has been found in over 80% of experimental studies, covering representatives of many of the animal phyla and extending from nematodes to amphibians. The inverse relationship between rearing temperature and adult size is most fully documented in the arthropods and, particularly, in the dipteran insects, with many studies on species of mosquito (eg van den Heuvel, 1963, Lyimo et al., 1992) and of the fruitfly, Drosophila (eg Alpatov, 1930, Robertson, 1959, Delcour and Lints, 1966, David and Clavel, 1969, Powell, 1974, Masry and Robertson, 1979, Coyne and Beecham, 1987, Partridge et al., 1994a, Partridge et al., 1994b, Noach et al., 1996).

Insect body size is determined by the dimensions of the surface epidermis that secretes the exoskeleton and this, in turn, is set by the number and the size (strictly, the surface area) of the epidermal cells. The development of flies, such as Drosophila, includes a dramatic pupal metamorphosis in which the larval epidermis of the body segment dies and is completely replaced by separate populations of adult (imaginal) cells that coalesce to form the continuous adult epidermis. During the first half of embryonic development, the segments are established and grow by cell division, while small groups of cells in particular locations within the segment become specified as imaginal primordia (Cohen et al., 1993, Cohen, 1993). All cell division then stops and thereafter the larval segment epidermis grows only by the cells becoming polyploid and greatly enlarged. In the head and thoracic segments of the young larva, cell division resumes within the invaginated imaginal discs. A wing imaginal disc, for example, grows from about 20 to 50 000 cells between the mid first and late third larval instars, with a cell cycle time of around 8 hours (Bryant and Levinson, 1985). The wing disc evaginates just after pupariation, fuses with adjacent discs and undergoes more cell division in the early pupa (Schubiger and Palka, 1987). Finally, the epidermis secretes adult cuticle, forming one side of the adult dorsal mesothorax and one wing. Similarly, a leg disc forms ventral mesothorax and the leg. Each side of the adult abdominal segment derives from four small groups of imaginal cells, the histoblast nests. Unlike the discs, however, these imaginal primordia remain in the plane of the polyploid larval epidermis and the cells do not divide during larval stages, although they do increase greatly in size (Madhavan and Schneiderman, 1977). Histoblast cell division starts shortly after pupariation and proceeds rapidly in the early pupa, the nests spread and they sequentially replace the surrounding larval epidermis, so that adjacent nests become fused (Madhavan and Madhavan, 1980). By mid pupal stage, cell division has ceased and the adult epidermis is complete.

Several previous studies on Drosophila melanogaster have shown that development at a temperature below the standard 25°C reduces growth rate, extending the duration of both the larval and pupal stages (eg Partridge et al., 1994a). The weight of the mature larva is increased, however, as is the weight of the subsequent adult and the size of its wing, thorax and leg (eg David and Clavel, 1969, Partridge et al., 1994a, Partridge et al., 1994b). A change in adult size could result from changes in the number and/or the size of the epidermal cells. This issue can be readily resolved in the wing blade, where each cell secretes a single trichome (Dobzhansky, 1929), and density counts have shown that rearing temperature influences wing size through effects on the size of the cells, with little or no change in cell number (Alpatov, 1930, Robertson, 1959, Masry and Robertson, 1979, Partridge et al., 1994b). From experiments in which the temperature was shifted at times during postembryonic development, there are indications that the period of temperature-sensitivity may differ between the thorax and the wing (Masry and Robertson, 1979, David et al., 1983).

In the present experiments, we have shifted cultures of Drosophila to low (16.5°C) or to high (29°C) temperature at regular intervals through larval and pupal stages, and have analysed the effects on adult size. We have studied the wing and dorsal mesothorax (both derived from the wing disc) and also an abdominal segment, in order to relate the timing of temperature sensitivity to the different growth patterns of the imaginal primordia and to larval feeding, growth and pupariation.

Section snippets

Materials and methods

The flies were derived from a laboratory stock of Drosophila melanogaster that was originally collected in Brighton (UK) fruit market in 1984 and subsequently maintained at 25°C in large population cages. The parents of experimental animals were reared in standard, low density conditions from eggs laid on yeasted dishes which were placed in the population cage. Eggs were then transferred onto yeasted Lewis medium in 300 ml culture bottles (approximately 300 eggs per culture) and reared at 25°C

Temperature and thorax size

The adult mesothorax is much larger in female Drosophila than in the males. In each sex, however, mesonotum length was increased by low temperature (16.5°C) and decreased by high temperature (29°C) experienced during development (Fig. 2). The effect on thorax size depended on the proportion of postembryonic development spent at the non-standard temperature, hence on the time of the temperature-shift. The earliest shifts, at approximately 2 h after hatching, resulted in an approximately 5% change

Discussion

An effect of rearing temperature on growth rate and body size appears to be characteristic of ectotherms. There are well-documented exceptions (eg Lamb and Gerber, 1985, Roe et al., 1980) but the typical pattern, exemplified by Drosophila, is that growth rate is positively correlated, but body size is negatively correlated, with temperature during development (Atkinson, 1994).

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