DISCUSSION
Our understanding of how organisms
respond to predation risk has traditionally focused on a small number of
specific traits in only a few environments. Recent advances have moved
the standard of plasticity research to a multi-trait approach including
morphology, life history and behaviour along environmental gradients.
This has been complemented by a growing appreciation that morphometric
analyses applied to organism shape can provide added value to analyses
of phenotypic plasticity.
Here, building on this growing use of morphometrics in plasticity
research, we evaluated ‘shape’ plasticity among three genotypes ofD. pulex exposed to a gradient of six levels of predation risk.
Our objective was to use morphometric shape as a ‘summary’ trait
affected by responses to predation risk in life history and morphology
to evaluate several hypotheses about the impact of predation risk on
whole organism plasticity. Our motivation was linked to size selective
predation theory and work on the response of fish to predation risk
where size and shape are both linked to survival . We found that theD. pulex response to predation risk involves both modular and
integrated changes, with changes in the inducible neckteeth defence
linked to changes in head and body shape. This suggests that there is a
complex response to predation, including strong developmental
correlations in how Daphnia body plans are organised.
Our first set of results from the trajectory analysis showed how
morphology changed in response to a gradient of predation risk. In
accordance with previous studies of the inducible defence and our
initial hypothesis, we found that head width (neck-change) increases
along the gradient of predation risk . Also, we found that head height
varied among clones and body width (belly-bulge) was a non-linear
feature of change. This last result is contrary to our hypothesis
derived from the fish literature; we predicted that body width would
decrease along a rising gradient of predation risk linked to
swimming/evasion, but in reality, body width varies regardless of the
level of predation risk.
Our second set of results from the modularity and integration tests
showed evidence for modularity between the head and the body, as
expected, but also integration across these two body regions. This
suggests that there is a high level of coordination within the head and
the body, but there is also an integrated ‘trade-off’ among aspects of
the body plan under predation risk. Specifically, as we predicted, as
the neck region enlarges, the back moves higher, the tail is drawn
towards the front of the body and the snout shifts backwards. Contrary
to our other hypothesis, we found no evidence for modularity in the back
and front regions. However these two groupings of landmarks are
integrated in their response to predation risk, which is likely to be
derived from the modular and integrated response of the head and lower
body.
It is well-documented that the inducible defence of D. pulexincreases in response to higher levels of predation risk . This
morphological defence has long been hypothesized to form part of a
whole-organism response to predation that includes changes in size and
life-history traits linked to the allocation of energy to growth,
defence morphology and reproduction .
In comparison, there has been some work on body width, which is another
key aspect of shape that we analysed, but it is unclear what role this
plays in the response to predation risk. Previous studies have used
linear morphometrics to show a relatively small increase in body width
in defended compared to undefended morphs of D. pulex andD. magna which suggests that body width may play a minor role in
the response to predation. In support of this, it has been shown that
body width is a better predictor for prey size range in Chaoborusthan body length . Chaoborus usually swallows prey that cannot be
deformed only if its diameter is not wider than the larva’s head capsule
diameter . The increase in body depth might additionally make prey
handling for the larvae more difficult. Alternatively, the increased
body width in defended compared to undefended morphs may result from the
increase in strength, and possibly thickness, of the carapace . Similar
to the changes in body width, variation in head height, something
revealed in our analysis, has not been well-documented, but may be
linked to hydrodynamics .
In this study, there was both a modular and whole-organism, integrated
response to predation (sensu . This is entirely possible, as
modularity and integration are not two ends of a continuum, but
represent two mutually compatible destinations of selection. It is
commonly thought that the evolution of modularity and integration is
linked to trait functionality. In the case of modularity, there can be
selection for ‘variational adaptation’, where traits that often respond
together to environmental pressures, such as predation risk, are
integrated into one module, and traits that rarely need to be changed at
the same time are packed into another module . This may explain why
changes in the head of D. pulex , which form the main response to
predation risk, are relatively independent of changes in the body.
Possible functions of the observed integration could be for carapace
stability or an improved escape response . Alternatively, integration
could increase fitness by co-ordinating the response of multiple traits
to spatial and/or temporal variation in the environment. Regardless, our
results deliver strong support for the existence of developmental
constraints (correlations) that are worth investigating to understand
the nature of predator induced phenotypic plasticity.
Shape variation in response to predation risk has not previously been
studied in D. pulex . In this study, we exposed D. pulex to
six levels of predation risk and evaluated shape plasticity using
geometric morphometrics and phenoptypic trajectory analysis. We now have
a better understanding that D. pulex shape is a multivariate
response to predation risk, that there is genetic variation in this
response and that the responses can be both modular and integrated, with
associated adaptive and non-adaptive (constraint) hypotheses in need of
further evaluation. Thus, there are two clear ‘next-steps’. The first is
to establish the adaptive benefit/costs of shape change and variation.
The second is the molecular ecology of the developmental constraints.
The availability of genomic tools, the clonal nature of Daphnia ,
well-established experimental protocols and recent high throughput image
analysis are an outstanding platform for future research.