Do replicates of independent guppy lineages evolve similarly in a predator‐free laboratory environment?

Abstract

The Trinidadian guppy is emblematic of parallel and convergent evolution, with repeated demonstrations that predation regime is a driver of adaptive trait evolution. A classic and foundational experiment in this system was conducted by John Endler 40 years ago, where male guppies placed into low‐predation environments in the laboratory evolved increased color in a few generations. However, Endler's experiment did not employ the now typical design for a parallel/convergent evolution study, which would employ replicates of different ancestral lineages. We therefore implemented an experiment that seeded replicate mesocosms with small founding populations of guppies originating from high‐predation populations of two very different lineages. The different mesocosms were maintained identically, and male guppy color was quantified every four months. After one year, we tested whether male color had increased, whether replicates within a lineage had parallel phenotypic trajectories, and whether the different lineages converged on a common phenotype. Results showed that male guppy color generally increased through time, primarily due to changes in melanic color, whereas the other colors showed inconsistent and highly variable trajectories. Most of the nonparallelism in phenotypic trajectories was among mesocosms containing different lineages. In addition to this mixture of parallelism and nonparallelism, convergence was not evident in that the variance in color among the mesocosms actually increased through time. We suggest that our results reflect the potential importance of high variation in female preference and stochastic processes such as drift and founder effects, both of which could be important in nature.

Sensory‐based quantification of male colour patterns in Trinidadian guppies reveals no support for parallel phenotypic evolution in multivariate trait space

“…Nor is it found consistently across the HP to LP transition within rivers. Although the lack of stronger patterns may seem surprising, we note that multiple previous guppy studies have also reported similarly inconsistent differences across regimes within rivers using transplant (Dick et al, 2018; Kemp et al, ,2009, 2018) and predator‐manipulation experiments (Gotanda et al, 2019). More generally, we stress that our conclusions relate to the phenotype as defined here from the QCPA pipeline, and it is not our contention that previous studies using different colour traits are incorrect.…”

“…For example, low predation risk is thought to allow the evolution of larger colour spots on the body (Haskins et al, 1961). However, in a recent study, parallel increases in the relative area and number of melanic (black) spots as well as their size occurred across mesocosms lacking predators, but other colour traits changed inconsistently (Gotanda et al, 2019).…”

Biting kinematics do not differ between ecologically divergent populations of Trinidadian guppies

“…We suggest that morphological divergence may be more complex than what is represented by simple morphometric measurements, and this may explain our result. In fact, a few other studies have also found no relationship between predation regime and body shape for guppies (Alexander et al, 2006;Burns et al, 2009;Gotanda et al, 2019) and Burns et al, (2009) suggested that factors influencing body shape may be more complex than predation level alone. Since we collected fish from known HP/LP natural populations, we suggest that our fish are most likely representative of guppies more broadly, and that we may have been more likely to discover differences if we had used more detailed techniques (geometric morphometrics) or accounted for additional ecological factors.…”

Revisiting old truths: The evolution of male coloration in guppies as a function of predation

“…Other studies have found results that are consistent with Endler's original work, although many studies were conducted on the Marianne River drainage (Millar et al 2006; Gotanda & Hendry 2014), where both Yong et al (2021) and Valvo et al (2021) found evidence for large changes in conspicuousness. Multiple transplant studies have found that male coloration changes when predation risk is altered (Endler, 1980; Gordon et al, 2015; Gotanda et al, 2019; Kemp et al, 2018).…”

“…Subsequent work by Endler (1978, redrawn in Figure 2) suggested that males from low predation populations were more “conspicuous” to females, having more numerous and larger spots on their bodies. Introduction experiments, where guppies were transferred from high to low predation sites, found that guppies released from predation quickly evolved more/larger colour elements, although whether these were “black” or “orange” or “iridescent” varied (Endler, 1980; Gordon et al, 2015; Gotanda et al, 2019; Kemp et al, 2018). This work on guppy coloration is featured in multiple science curricula designed to illustrate trade‐offs in evolution (Blattner et al, 2012; Kane et al, 2018; Evolution, 2001).…”