Estimates of integration, mean trait correlation, constraints, and
flexibility may limit pupfish diversification on San Salvador Island
Our results suggest that greater independence in trait variation is
associated with diversification in this system. The P matrix of the SSI
generalist-only group had significantly greater estimates of integration
and mean squared correlation between craniofacial traits, higher
estimates of constraints, and lower estimates of flexibility– all
measurements that can be interpreted as proxies for independence between
traits (Table 2; Figure 6). For example, we observed the highest
correlation between cranial traits in the SSI generalist-only group,
which indicates that the mechanisms producing shifts in trait values for
one trait are likely to affect the values for many others, which
ultimately may limit the phenotypic space that these populations can
access (Goswami & Polly, 2010). Furthermore, the constraint and
flexibility estimates for the SSI generalist-only group suggest that
they are limited, specifically in comparison to Caribbean and SSI
radiating group, in their ability to respond to and align with a wide
range of selection gradients. This limited ability to respond to a range
of selection gradients, may explain why these populations are exposed to
similar environmental conditions, yet have not evolved the snail- and/or
scale-eater specialists found in other lakes.
Other empirical studies also suggest that independence across many
biological levels may be positively associated with diversification.
Greater amounts of gene duplication, larger ratios of
nonsynonymous:synonymous mutations, and lower levels of covariation
between morphological traits, have all been suggested as integral to
diversification in some African cichlid radiations (Brawand et al.,
2014; Machado et al., 2014; Selz et al., 2014), and represent
independence at both the genetic and morphological levels. Similarly,
Ravinet et al. (2014) suggest that populations of three-spined
stickleback from the Japan Sea have not colonized freshwater habitats
and subsequently diversified, as many of the closely related Pacific
freshwater populations have done, specifically due to the increased
correlation between their morphology and dietary niche. Lastly, the
flexible stem hypothesis suggests that the divergence within adaptive
radiations emerges from plastic phenotypic variation in an ancestral
population (West-Eberhard, 2003). Through this lens, the properties of
the Caribbean P-matrix could be viewed as being plastic (i.e., low
levels of constraints, high levels of flexibility, and low
respondability)—estimates which remain largely the same in radiating
groups and which have shifted in non-radiating groups. Other empirical
studies, however, have found mixed results regarding the relationship
between plasticity and diversification. Navolón et al. (2020) observed
that higher integration, which may imply lower levels of plasticity,
likely helped produce the diversity seen in the adaptive radiations of
Darwin’s finches and Hawaiian honeycreepers. On the other hand, lower
levels of integration in brown trout allowed them to diversify into a
new ecological niche when faced with a new selective pressure (Závorka
et al., 2017). These results support that independence and flexibility,
either within or between, molecular, morphological, and/or behavioral
traits contributes to a group’s ability to diversify. The findings
presented in this study further support this conclusion.