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

Abstract

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.

Fig 1.

Simplified biosynthetic pathway from acetate to triglyceride and phospholipid, indicating where radiolabeled sodium acetate and palmitic acid enter the pathway.

Fig 2.

Amount of radiolabeled [1-¹⁴C]acetate or [1-¹⁴C]palmitic acid incorporated into triglyceride or phospholipid in LW(f) or SW G. firmus on day 5 of adulthood. Trigly, triglyceride; Phos, phospholipid. Block refers to independent selection trial (see Materials and Methods). The asterisks in parentheses indicate results of paired t tests (***, P < 0.005; *, P < 0.05). Values in all panels are means (±SEM) based on 20–28 individuals. On day 0, mean triglyceride or phospholipid dpm (from [1-¹⁴C]acetate) did not differ significantly between morphs within any block (P > 0.1 for all ANOVAs) or across blocks (P > 0.1 for paired t tests). Grand mean dpm (means across the three blocks) are as follows: triglyceride, 9,606 ± 1,814 [LW(f)] and 9,328 ± 1,861 (SW); phospholipid, 3,030 ± 139 [LW(f)] and 2,861 ± 188 (SW).

Fig 3.

(Upper) Amounts of biosynthesized triglyceride (T) and phospholipid (P) found in both ovaries (Ovary), whole body minus ovaries (Soma), and whole bodies (Total Body = Soma plus Ovary) of morphs of G. firmus from block 1. [1-¹⁴C]Acetate was the radiolabel used. (Lower) Effect of methoprene, a JH agonist, on the biosynthesis of triglyceride and phospholipid from [1-¹⁴C]acetate or [1-¹⁴C]palmitic acid in the LW(f) morph of G. firmus from block 1. Values are means (±SEM) based on 7–8 individuals (Upper) or 22–26 individuals (Lower) measured on day 5 of adulthood.