Anthony J. Zera

The physiology of life-history trade-offs: experimental analysis of a hormonally induced life-history trade-off in Gryllus assimilis.

Adult Gryllus assimilis given an analog of juvenile hormone exhibited reduced flight muscles and enlarged ovaries similar to those found in naturally occurring flightless individuals of species that are polymorphic for dispersal capability. Control and hormone‐treated (flightless) G. assimilis did not differ in the amount of food consumed or assimilated on any of three diets that differed in nutrient quantity. Thus, enhanced ovarian growth of flightless individuals resulted from increased allocation of internal nutrients to reproduction (i.e., a trade‐off) rather than from increased acquisition of nutrients. Compared with flight‐capable controls, flightless G. assimilis also had reduced whole‐organism respiration, reduced respiration of flight muscles, and reduced lipid and triglyceride (flight fuel) reserves. These differences are remarkably similar to those between naturally occurring flightless and flight‐capable morphs of other Gryllus species. Results collectively suggest that the increased allocation of nutrients to ovarian growth in flightless G. assimilis and other Gryllus species results from reduced energetic costs of flight muscle maintenance and/or the biosynthesis or acquisition of lipids. Reduction in these energetic costs appears to be an important driving force in the evolution of flightlessness in insects. Respiratory metabolism associated with flight capability utilizes an increasing proportion of the energy budget of crickets as the quantity of nutrients in the diet is decreased. This leads to a magnification of greater ovarian growth of flightless versus flight‐capable individuals on nutrient‐poor diets.

Flight‐Muscle Polymorphism in the Cricket Gryllus firmus: Muscle Characteristics and Their Influence on the Evolution of Flightlessness

Flight muscles of the cricket Gryllus firmus are polymorphic, existing as pink or white phenotypes. White muscles are smaller in size, have reduced number and size of muscle fibers, and have reduced in vitro enzyme activities and respiration rates relative to pink muscles of newly molted, fully winged adults. G. firmus is also polymorphic for wing length. All newly molted long‐winged adults exhibited the pink‐muscle phenotype, while most newly molted short‐winged adults exhibited the white‐muscle phenotype, which resulted from arrested muscle growth. As long‐winged adults aged, fully grown pink muscle was transformed into white muscle via histolysis. The substantially higher respiration rate of pink muscle likely contributes to the elevated whole‐organism respiration rate of long‐winged females, which has been documented previously and which is thought to divert nutrients from egg production. Histolyzed white flight muscle from long‐winged crickets also exhibited significantly elevated respiration rate and enzyme activities compared with underdeveloped white muscle from short‐winged adults, although these differences were not as great as those between pink and white muscles. Fecundity was much more elevated in females with white versus pink flight muscles than it was in females with short versus long wings. The fitness gain resulting from flightlessness has typically been estimated in previous studies by comparing enhanced egg production of short‐winged and long‐winged females, without considering the influence of flight‐muscle variation. Our results suggest that the magnitude of this fitness gain has been substantially underestimated.

Differential allocation of resources underlies the dispersal-reproduction trade-off in the wing-dimorphic cricket, Gryllus rubens

The cricket, Gryllus rubens (Orthoptera, Gryllidae), exists in natural populations as either a fully-winged (LW), flight-capable morph or as a short-winged (SW) morph that cannot fly. The SW morph is substantially more fecund than the LW morph. In this study we report on the physiological basis of this trade-off between flight capability and fecundity. Results from gravimetric feeding trials indicate that LW and SW morphs are equivalent in their consumption and digestion of food. However, during the adult stage, the LW morph is less efficient in converting assimilated nutrients into biomass. This may be a consequence of the respired loss of assimilated nutrients due to the maintenance of functional flight muscles in the LW morph. In both morphs the gross biomass devoted to flight muscles does not change significantly during the first 14 days of adult growth while there is a significant biomass gain in ovarian tissue mass during the same period. SW morphs have vestigial flight muscles and gain substantially more ovarian mass relative to the LW morphs. These data are consistent with a trade-off between flight muscle maintenance in the LW morph and ovarian growth in the SW form. This is the first evidence for a life-history trade-off that has a physiological basis which is limited to the allocation of acquired and assimilated nutrients within the organism.

Differential lipid biosynthesis underlies a tradeoff between reproduction and flight capability in a wing-polymorphic cricket

The biochemical basis of life-history tradeoffs is a poorly studied aspect of life-history evolution. We used radiotracer and endocrine approaches to investigate the extent to which morphs of a wing-polymorphic insect differ in the biosynthesis of lipid classes important for dispersal capability vs. reproduction (ovarian growth). The flight-capable genotype of Gryllus firmus biosynthesized a greater amount of total lipid and triglyceride (main flight fuel), which was preferentially allocated to somatic tissue during early adulthood. By contrast, the flightless genotype biosynthesized a significantly greater amount of phospholipid (important in egg development), which was preferentially allocated to ovaries. Topical application of a juvenile-hormone mimic to the flight-capable morph caused it to express all aspects of lipid metabolism seen in the flightless morph. Differences in biosynthesis between morphs (i) occur coincident with 100–400% greater ovarian growth in the flightless morph, (ii) result from alterations of both de novo biosynthesis of fatty acid and downstream partitioning of fatty acids into triglyceride vs. phospholipid, and (iii) possibly result from genetically polymorphic hormonal regulators with negative pleiotropic effects on lipid biosynthesis and ovarian growth. The present study provides direct documentation of genetically based alterations of in vivo flux through pathways of intermediary metabolism leading to the differential production of end products central to the specialization of phenotypes for alternate life histories.

The Endocrine Regulation of Wing Polymorphism in Insects: State of the Art, Recent Surprises, and Future Directions

Abstract The endocrine mechanisms controlling the development and reproduction of flight-capable (long-winged) and flightless (short-winged or wingless) morphs of wing-polymorphic insects have been intensively investigated. The “classical model,” put forward in the early 1960s, postulates that morph-specific differences in development and reproduction are caused by variation in the titers of juvenile hormone (JH) and/or ecdysone. Despite decades of study, the importance of these hormones in regulating wing polymorphism in aphids and planthoppers remains uncertain. This uncertainly is largely a consequence of technical and size constraints which have severely limited the types of endocrine approaches that can be used in these insects. Recent studies in wing-polymorphic crickets (Gryllus) have provided the first direct evidence that the in vivo blood titers of juvenile hormone and ecdysone, and especially the activity of the JH regulator, juvenile hormone esterase, differ between nascent morphs. Morph differences are largely consistent with the classical model, although some types of data are problematic, and other explanations are possible. Adult morphs differ dramatically in the JH titer but titer differences are more complex than those proposed by the classical model. Detailed endocrine information is thus far available only for a few species of crickets, and the hormonal control of wing polymorphism for insects as a whole remains poorly understood. Future studies should continue to investigate the role of JH and ecdysteroids in morph development and reproduction, and should expand to include studies of morph-specific differences in hormone receptors and neurohormones.

DIFFERENCES IN SURVIVORSHIP, DEVELOPMENT RATE AND FERTILITY BETWEEN THE LONGWINGED AND WINGLESS MORPHS OF THE WATERSTRIDER, LIMNOPORUS CANALICULATUS

Species of waterstriders (Gerridae: Hemiptera) exhibit a remarkable diversity in degree of winglessness (Vepsalainen, 1978; Calabrese, 1980; Zera, 1981). Some species consist exclusively of fully-winged individuals, while other species are composed almost exclusively of wingless individuals; many species exhibit the intermediate case of wing polymorphism and consist of various proportions of fully-winged, short-winged and/or wingless morphs. Wing-polymorphic species often exhibit dramatic spatial and/or temporal variation in morph ratios, both among populations of the same species and among species. Because of this diversity, waterstriders, especially wing polymorphic species, are ideal candidates for the study of the evolution of winglessness (or conversely, the evolution of dispersal). One of the major questions in the study of the evolutionary forces which influence wing polymorphism concerns fitness differences among the morphs. In many non-gerrids, dramatic differences between the fully-winged and the shortwinged or functionally equivalent (Anderson, 1973) wingless morph have been documented in a variety of fitness-associated traits (for reviews, see Harrison, 1980; Dingle, 1982). These include differences in such traits as survivorship under stress, duration of larval or nymphal development, age of first reproduction, and fecundity. Moreover, one of the most important results of these studies is the demonstration that differences in fitness traits are often consistently associated

The Metabolic Basis of Life History Variation: Genetic and Phenotypic Differences in Lipid Reserves among Life History Morphs of the Wing-Polymorphic Cricket, Gryllus firmus

The flight-capable morph of the wing-polymorphic cricket, Gryllus firmus, accumulated a substantially greater quantity of total lipid and triglyceride, compared with the obligately flightless morph, during the first five days of adulthood. Increased lipid accumulation in the flight-capable morph was genetically based, and was produced when ovarian growth is substantially reduced in that morph. Temporal changes in lipid levels suggest that the higher triglyceride reserves in the flight-capable morph fed a high-nutrient diet were produced by elevated lipid biosynthesis. By contrast, on a low-nutrient or high carbohydrate diet, increased lipid levels in the flight-capable morph appeared to result primarily from decreased lipid utilization. Increased biosynthesis or retention of triglyceride (the major flight fuel in Gryllus) by the flight-capable morph may significantly divert nutrients from egg production and hence may be an important physiological cause of its reduced ovarian growth. The obligately flightless morph allocated a greater proportion of total lipid to phospholipid than did the flight-capable morph. No functionally-significant differences in total lipid or triglyceride were produced between morphs during the last nymphal stadium. A second flightless morph, derived from the flight-capable morph by histolysis of flight muscles during adulthood, also had reduced amounts of total lipid and triglyceride but increased ovarian growth compared with the flight capable morph on the standard (high-nutrient) diet. Important qualitative and quantitative aspects of lipid metabolism differ genetically between the flight-capable and flightless morphs of G. firmus and likely contribute importantly to their respective adaptations for flight capability vs. reproduction. This is the first study to document genetically-based differences in energy reserves between morphs of a complex (phase, caste, flight) polymorphism in which morphs also differ genetically in key life history traits.

Genetic Structure of Two Species of Waterstriders (Gerridae: Hemiptera) with Differing Degrees of Winglessness

The Gerridae (Hemiptera: Insecta) is a worldwide family whose constituent species exhibit dramatic interand intraspecific variation in the degree of winglessness (Brinkhurst, 1960; Vepsaliiinen, 1978; Calabrese, 1979). At one extreme, the family contains species which are fully winged in all populations and during all seasons, while several species consist almost exclusively of wingless morphs over large geographical ranges and during all seasons. Many species exhibit the intermediate case of wing-polymorphism: the occurrence of various combinations of fully winged, partially winged and/or wingless morphs in the same population at the same time. Various wing-polymorphic species show differing patterns of spatial and/or temporal changes in morph ratios and patterns may vary both interand intraspecifically. The dramatic differences in frequency of winged morphs pose intriguing questions regarding the evolutionary forces responsible for degree of winglessness and the relationship between degree of winglessness and genetic structure of waterstrider species. One might expect genetic structure to be strongly influenced by degree of winglessness via reduction of flight dispersal ability and consequent reduced gene flow. Thus, species composed almost exclusively of wingless individuals should exhibit patterns of marked genetic differ-

Lipid, carbohydrate and nitrogen content of long- and short-winged Gryllus firmus: Implications for the physiological cost of flight capability

Abstract Concentrations of total lipid, triglyceride, soluble carbohydrate, total nitrogen and water were measured in the long-winged (LW) and short-winged (SW) morphs of the cricket, Gryllus firmus . In addition, the weights and composition of wings and oviposited eggs were compared between morphs. This was done to obtain information on the energetic cost of flight capability in the LW morph. Whole-cricket content (% dry mass) of triglyceride was significantly higher in LW vs SW individuals of both sexes. Since triglyceride is a likely flight fuel in G. firmus , the biosynthesis of elevated levels of this high energy substance in the LW morph may represent an important energetic cost of flight capability. The existence of such a cost is consistent with the elevated respiratory metabolism previously observed in LW vs SW G. firmus . A highly significant negative correlation was observed between triglycerides and non-triglycerides in LW but not SW crickets. This suggests that lipid biosynthesis may be operating under some constraint in the LW morph. Increased triglyceride biosynthesis may require a concomitant decreased biosynthesis of non-triglycerides. In contrast to the elevated triglyceride level in the LW morph, carbohydrate concentration was higher in the SW morph during early adulthood. Carbohydrate content also decreased with age in the SW but not in the LW adults. No differences were observed between morphs in (1) the total nitrogen or water contents of whole crickets, (2) the nitrogen content of wings or (3) the wet weight, dry weight, lipid content, or total nitrogen content of oviposited eggs.

Intermediary Metabolism and Life-History Trade-Offs: Differential Metabolism of Amino Acids Underlies the Dispersal-Reproduction Trade-Off in a Wing-Polymorphic Cricket

Although the differential flow of metabolites through alternate pathways of intermediary metabolism is thought to be an important functional cause of life‐history trade‐offs, this phenomenon remains understudied. Using a radiolabeled amino acid, we quantified genetic differences in in vivo amino acid metabolism between morphs of the wing‐polymorphic cricket Gryllus firmus that trade off early‐age reproduction and dispersal capability. Lines selected for the flight‐capable morph, which delays reproduction, oxidized a greater proportion of radiolabeled glycine and converted a greater amount into somatic lipid, mainly triglyceride (flight fuel). By contrast, lines selected for the flightless, reproductive morph converted a substantially greater proportion of glycine into ovarian protein. Compensatory interactions between amino acid and lipid metabolism make up a key aspect of specialization for dispersal versus reproduction in G. firmus: increased oxidation of amino acids by the flight‐capable morph spares fatty acid for enhanced conversion into triglyceride flight fuel. By contrast, increased oxidation of fatty acid by the flightless morph spares amino acids for enhanced biosynthesis of ovarian protein. Studies of amino acid and lipid metabolism in G. firmus currently represent the most detailed analyses of genetic modifications of intermediary metabolism that underlie a functionally important life‐history trade‐off found in natural populations.