The persistence and evolutionary consequences of vestigial behaviours

Abstract

Behavioural traits are often noted to persist after relaxation or removal of associated selection pressure, whereas it has been observed that morphological traits under similar conditions appear to decay more rapidly. Despite this, persistent non-adaptive, 'vestigial' behavioural variation has received little research scrutiny. Here we review published examples of vestigial behavioural traits, highlighting their surprising prevalence, and argue that their further study can reveal insights about the widely debated role of behaviour in evolution. Some vestigial behaviours incur fitness costs, so may act as a drag on adaptive evolution when that adaptation occurs via trait loss or reversal. In other cases, vestigial behaviours can contribute to future evolutionary trajectories, for example by preserving genetic and phenotypic variation which is later co-opted by selection during adaptive evolution or diversification, or through reemergence after ancestral selection pressures are restored. We explore why vestigial behaviours appear prone to persistence. Behavioural lag may be a general phenomenon arising from relatively high levels of non-genetic variation in behavioural expression, and pleiotropic constraint. Long-term persistence of non-adaptive behavioural traits could also result when their expression is associated with morphological features which might be more rapidly lost or reduced. We propose that vestigial behaviours could provide a substrate for co-option by novel selective forces, and advocate further study of the fate of behavioural traits following relaxed and reversed selection. Vestigial behaviours have been relatively well studied in the context of antipredator behaviours, but they are far from restricted to this ecological context, and so deserve broader consideration. They also have practical importance, with mixed evidence, for example, as to whether predator/parasite-avoidance behaviours are rapidly lost in wildlife refuges and captivity. We identify important areas for future research to help determine whether vestigial behaviours essentially represent a form of evolutionary lag, or whether they have more meaningful evolutionary consequences distinct from those of other vestigial and behavioural traits.

Decoupling of sexual signals and their underlying morphology facilitates rapid phenotypic diversification

“…Selective pressures may also be reversed, where a previously advantageous phenotype becomes strongly selected against (reversed selection; Rayner et al 2022). In Hawaiian populations of T. oceanicus, the arrival and proliferation of the fly changed the selective landscape so that net selection on ancestral song was reversed; selection from flies against males producing ancestral song may have allowed for multiple successful new morphs to become quickly established, as nearly any deviation from the previously optimal ancestral signal may increase male fitness (Figure 4B;Tinghitella et al 2021).…”

The evolutionary demise of a social interaction: social partners differ in the rate at which interacting phenotypes are lost

“…For this reason, it is important to understand how long such adaptive traits can persist at the population level if they are no longer routinely expressed. This is especially true for behavioural traits, which have been relatively under-studied in this context (Rayner et al, 2022).…”

“…However, the greater the net fitness costs, the more rapidly we would expect the mechanism for plasticity to be lost. There are then two possibilities -either there is genetic assimilation and the trait is constitutively expressed, independent of environmental conditions (DeWitt et al, 1998;Pigliucci et al, 2006;Robinson and Dukas, 1999;Scheiner and Levis, 2021;Snell-Rood et al, 2009;Waddington, 1953), or trait expression ceases altogether and the trait is lost (Lahti, 2006;Rayner et al, 2022). The latter possibility is the focus of our work here.…”

“…The capacity for any unexpressed trait to persist is thought to be due to a combination of adaptive and neutral processes (Lahti et al, 2009, Rayner et al 2022). Adaptive processes are involved because selection will act against the mechanisms that enable an unexpressed trait to be environmentally induced if there are associated costs with trait plasticity (DeWitt et al, 1998; Snell-Rood et al, 2018).…”

“…The costs could be outweighed by any fitness benefits accrued through the occasional expression of this trait. If there are no net costs, then the trait might persist – vestigially and non-adaptively (Rayner et al, 2022). However, the greater the net fitness costs, the more rapidly we would expect the mechanism for plasticity to be lost.…”