Phenotypic plasticity and diversity in insects

Abstract

Phenotypic plasticity in general and polyphenic development in particular are thought to play important roles in organismal diversification and evolutionary innovation. Focusing on the evolutionary developmental biology of insects, and specifically that of horned beetles, I explore the avenues by which phenotypic plasticity and polyphenic development have mediated the origins of novelty and diversity. Specifically, I argue that phenotypic plasticity generates novel targets for evolutionary processes to act on, as well as brings about trade-offs during development and evolution, thereby diversifying evolutionary trajectories available to natural populations. Lastly, I examine the notion that in those cases in which phenotypic plasticity is underlain by modularity in gene expression, it results in a fundamental trade-off between degree of plasticity and mutation accumulation. On one hand, this trade-off limits the extent of plasticity that can be accommodated by modularity of gene expression. On the other hand, it causes genes whose expression is specific to rare environments to accumulate greater variation within species, providing the opportunity for faster divergence and diversification between species, compared with genes expressed across environments. Phenotypic plasticity therefore contributes to organismal diversification on a variety of levels of biological organization, thereby facilitating the evolution of novel traits, new species and complex life cycles.

Figure 1.

Examples of horned beetles illustrating diversity and magnitude of horn expression in adult beetles: (a) Phanaeus imperator, (b) Eupatorus gracilicornis, (c) Onthophagus watanabei, (d) Golofa claviger and (e) Trypoxylus (Allomyrina) dichotoma.

Figure 2.

Examples of (a) complex-scaling relationships and (b) divergences in scaling relationships in horned beetles. (a) Examples of horn length–body size scaling relationships in the beetle genus Onthophagus: (i) linear scaling relationship of paired head horns in O. watanabei (males: open circles; females: open diamonds); (ii) broken scaling relationship of pronotal horn length in male O. binodis; (iii) S-shaped (sigmoidal) scaling relationship of paired head horns in male O. taurus (modified after Moczek 2009). (b) Examples of divergences in scaling relationships in the genus Onthophagus over a range of phylogenetic distances: (i) three Onthophagus species, which diverged approximately 20–38 Myr ago (O. taurus: open circles; O. nigriventris: solid diamonds; O. gazella: open triangles); (ii) divergences in scaling relationships between two sister species, O. taurus (open circles) and O. illyricus (solid circles), which diverged approximately 10 000 years ago (Pizzo et al. 2008); (iii) divergences in scaling relationships between three allopatric O. taurus populations established less than 40 years ago from a common Mediterranean ancestor (Eastern USA: open circles; Eastern Australia: grey circles; Western Australia: solid circles; modified after Moczek 2003).

Figure 3.

Trade-offs between investment into polyphenic expression of horns and canalized investment into copulatory organs in populations and species of Onthophagus beetles. (a) Horned male Onthophagus taurus. Arrows highlight horns and copulatory organ. (b) Relative investment into copulatory organ size as a function of relative investment into polyphenic horn expression in four different populations of O. taurus. Error bars represent one standard error. (c) Relative investment into copulatory organ size as a function of relative investment into horn size in 10 different Onthophagus species. Data are corrected for differences in body size. Modified after Parzer & Moczek (2008).