Evolution of adult male horn developmental phenotypes and character displacement in Xylotrupes beetles (Scarabaeidae)

Abstract

Character displacement that leads to divergent phenotypes between sympatric species has been hypothesized to facilitate coexistence and promote the accumulation of biodiversity. However, there are alternative evolutionary mechanisms that may also lead to the evolution of phenotypic divergence between sympatric species; one of the mechanisms is evolutionary contingency. We studied the evolution of the presence and absence of a major male horn phenotype, which may have ecological implications for promoting coexistence between sympatric beetles, across geographic populations from different Xylotrupes beetles. By using a previously published phylogeny with 80 Xylotrupes taxa, we estimated the transition rates between the two phenotypic states (i.e., presence vs. absence of a major male phenotype). Based on the estimated transition rates, we then simulated possible phenotypic outcomes between sympatric species. We found that sympatric species were equally likely to evolve the same versus distinct phenotypic states based on the estimated transition rates given the phylogeny. The empirically observed number of sympatric species showing different phenotypic states can be explained by evolutionary contingency alone. We discussed the importance of applying phylogenetic comparative methods when studying phenotypic evolution and more generally to investigate the effect of stochastic processes before making deterministic inferences.

Keywords: Xylotrupes; beetle horn; character displacement; evolutionary contingency; phylogenetic comparative method.

FIGURE 1

Examples of different adult male horn developmental phenotypes between distantly related sympatric (BE vs. XB; SOS vs. XFS) or between closely related allopatric (BE vs. SOS; SIA vs. SIAYN) Xylotrupes beetles. The population id of each examplar individual is in parentheses. Color arrows indicate denticles on cephalic (red) or thoracic (blue) horns. Species name in blue indicate species that have long‐horn male phenotypes

FIGURE 2

The population tree, geographic distribution (blue dots indicate sympatric distribution of multiple lineages), and adult male horn developmental phenotype (black or white dots on leaves of the population tree) of the studied Xylotrupes beetles. The Figure was made using the phylo.to.map function in phytools (Revell, 2012). The coordinate information was retrieved from a previous study (Huang & Knowles, 2018) and can be found in supplementary files

FIGURE 3

The maximum likelihood estimation of ancestral states and transition rates between states of adult male horn developmental phenotypes in Xylotrupes beetles

FIGURE 4

The expected number of sympatric species showing distinct male horn developmental phenotypes based on 1,000 simulations. The empirical accounts were shown using vertical dash red lines. Specifically, there were four confirmed cases of sympatric Xylotrupes species that exhibit distinct phenotypes; additionally, there were two uncertain cases where the phenotypic state for one or both species from sympatry cannot be determined. Therefore, the actual accounts of sympatric species with different phenotypes may range from 4 to 6