Univariate responses in multicomponent signals
In nature, correlational selection may be quite common (Svensson et al.,
2021) and sexual signals are often found to be subject to multivariate
stabilizing and directional selection (Bentsen et al., 2006; Blankers et
al., 2015; Brooks et al., 2005; Devigili et al., 2015; Fisher et al.,
2009; Gerhardt and Brooks, 2009; Hine et al., 2011; Oh and Shaw, 2013;
Ryan and Rand, 2003; Tanner et al., 2017). In our experiment, we applied
a univariate selection gradient on the relative amount of Z11-16:OAc to
consider the evolvability of multivariate traits to univariate selection
gradients. We justified this univariate selection based on the found
geographic variation in the relative amount of Z11:16OAc in H.
subflexa . Females are likely specifically selected for higher rates of
acetates to avoid heterospecific mate attraction in regions where the
congener H. virescens occurs (Groot et al., 2009a).
Our observed selection response shows that there are no phenotypic or
genetic constraints to the evolution of Z11-16:OAc (or the other
acetates), as we reached similar or even higher levels of divergence
compared to those observed across the range of H. subflexa . After
10 generations in our selection experiment, the high line individuals
had on average almost 20% more Z11-16:OAc compared to the low line (Fig
2E), while H. subflexa populations in the eastern US were found
to have blends with up to 10% more Z11-16:OAc compared to populations
in the south-western US and Mexico (Groot et al., 2009a). The selection
response that we found was also surprisingly univariate, as only the
three acetate esters and none of the other components showed divergence
between the high and low lines. This indicates that the acetates can
evolve independently from the other components. This is surprising, both
in the context of the observed genetic correlations in the starting
population and in later generations (Fig 4) and in the context of what
is known about the shared biochemical pathways across the pheromone
components (Groot et al. 2009a; Fig 1). However, it is not an uncommon
result of artificial selection experiments (Hill and Caballero, 1992;
Saltz et al., 2017), including for sexual signals (Ritchie and Kyriacou,
1996). Thus, genetic correlations among sexual signal components may
quickly dissolve in the absence of correlational selection, which likely
facilitates their evolution on short time scales in response to
directional selection.
We acknowledge that our study does not include replicate lines in the
experiment. This is because each selection line consisted of hundreds of
single pair matings per generation, as H. subflexa is highly
sensitive to inbreeding. We thus needed to maintain large populations of
individuals that are mated in pairs and also individually reared to
avoid cannibalism, which makes these experiments very laborious.
Therefore, we chose to rear two lines in separate directions rather than
two replicates of only the high or low line. The fact that we found
parallel results between the lines in the selection response both in
phenotypic means and genetic covariances lends confidence to the
patterns observed. However, we do avoid drawing conclusions based on
differences between the lines, because these can both reflect
differential selection effects or sampling variance.