4. Individual and population fitness and some ramifications
Relationships between individual and population fitness in this
connection can be problematic. Population fitness depends not just on
the metric values for the fitness traits in its habitat which determine
individual fitness, but also on the amount of heritable variation for
those traits. In the poplar case, key adaptive traits in the wild would
include pathogen resistance, timing of seasonal growth, and the sexual
reproductive potential that allows genetic selection to operate. Thus,
the impact of some ill-adapted segregants can be outweighed by a
concurrent incidence of segregants that excel their parents’ fitness,
since the latter contribute most to the parentage of the next
generation. However, with pathogens involved, population fitness can be
complicated by the nature of infection processes. With a ‘polycylic’
pathogen, there can be both reinfection from within the host individual
and cross-infection between individuals. For instance, where pathogens
impair fitness, an individual becoming deciduous gains little or no
protection if the population remains evergreen and can thereby provide a
continuous supply of inoculum. In this way, becoming deciduous is
unlikely to be advantageous, unless either this results in asynchrony
between the window of host susceptibility and presence of inoculum or
individuals are too sparse to favour cross-infection. An individual
becoming evergreen, however, might impair the fitness of the rest of the
population through producing a continuous supply of inoculum, unless it
suffers so badly from internal reinfection as to incur selective
elimination. To meet that condition, internal reinfection would
presumably need to predominate strongly over cross-infection between
individuals, which may be common with polycyclic infection.
Becoming evergreen could require evolution of enhanced pathogen
resistance and/or some more direct fitness advantage of the habit.
Natural selection for resistance may be limited by ‘selective
opportunity cost’ whereby the fitness gains from additional resistance
are in trade-off with the fitness gains from responses to other
selective pressures. Some of those gains, it may be noted, will be
needed to make good the decay of non-additive genetic components of
fitness that occurs upon sexual reproduction. Given the dynamic nature
of biotic interactions, along with pathogen mutations, natural selection
for ecological fitness can be expected to entail a “red queen” model
(Van Valen 1973) requiring endless genetic shifts to maintain fitness.
With long-lived perennials, however, such shifts may occur most readily
within generational cohorts, during lifespans. With the complex and
highly dynamic poplar rust pathosystem, poplar plantations have proved
notoriously vulnerable to pathotype mutations (e.g. Persoons et al.
2014). Such plantations are typically monoclonal, which makes them
convenient to produce and manage. Present understanding of pathosystems
suggests that natural populations of poplars, reproducing by seed, might
be expected to be more resilient towards the rusts. However, fully
functioning natural populations, which would provide a good basis for
comparison, are becoming increasingly scarce.
It must be noted that the biotic vulnerability of poplar plantations,
based on species that are Melampsora hosts, contrasts with the
biotic resilience of natural stands of American (or trembling) aspen
(Popiulus tremuloides Michaux) which are typically monoclonal
(Latutrie et al. 2015). The aspen, with different pathogens, is
evidently involved in very different pathosystems.
5. Pre-adaptive relationships ?
As indicated above, seasonal timing of phenological events may serve as
defence against pathogens through avoidance of infection seasons while
the plant is vulnerable. Alternatively, the timing may be a source of
vulnerability. This seems evident in some cases of freshly introduced
pathogens, rather than in historically co-evolved cases. With Dutch elm
disease, caused by ascomycete fungi Ophiostoma spp, early bud
burst and flushing, while possibly incurring climatic vulnerability, can
evidently avoid the height of the infection season (Ghelardini &
Santini 2009). With sudden oak death, caused by Phytophthora
ramorum Werres et al., host vulnerability has been linked to timing of
bud burst and onset of cambial activity in the hosts (Dodd et al. 2008).
Similarly, the pathogen Austropuccinia psidii (G. Winter)
Beenken, a rust affecting a wide range of hosts in the Myrtaceae that
has invaded parts of Asia and the Pacific, can only infect actively
flushing host tissues (Beresford et al. 2020). In each case, invasive
pathogens appear likely to place strong selective pressures on the
phenology of native host populations, and understanding the potential
for adaptive responses appears to be worth further study.
6. Concluding
We propose that pathogens can be strong evolutionary drivers of seasonal
phenology, especially in respect of deciduousness. This appears to be
largely novel. Some evidence is given for our proposal for deciduousness
in a temperate zone. In the tropics, the proposal is made for want of
any other satisfactory explanation. Other examples are given of how
pathogens may influence seasonality of shoot flushing, where simple
climatic explanations seem inadequate. We suggest that evolutionary
barriers can operate against a shift from a deciduous to an evergreen
habit in some temperate-zone cases.
For herbivory we have proposed that predator satiation may operate as an
evolutionary driver in addition to purely climatic adaptation to the
occurrence of winters. Herbivory is also proposed as an evolutionary
constraint on growing or flowering seasons. For the tropics, where
climates are largely characterised by wet and dry seasons, predator
satiation has already been implicitly identified as a quite common
evolutionary driver of seasonal phenology.
Ontogenetic phenology appears strongly influenced evolutionarily by
biotic factors, including both herbivory and pathogens.
How a particular situation plays out will depend on many factors,
notably the general climatic context and the constraints it imposes
(along with other environmental factors), and the nature of biotic
pressures, viz pathogens and/or herbivory. More specifically, the
factors for pathogens involve the reproductive biology of pathogens
including seasonality; the host plant ecology, in the scale from highly
gregarious to essentially solitary; and the genetic systems of both host
and pathogens. For herbivory, they include the life cycles and seasonal
abundance of insects, along with the nature and abundance of vertebrate
browsers. Not to be ignored are interactions with other plants in the
ecosystem and among herbivores.
Influences of climate are both direct and indirect, the latter category
involving how much climate favours pathogens and herbivores. With
pathogens, there is the classic ‘triangle’ of interactions involving
host, pathogen and the environment, so the direct and indirect
evolutionary influences are in some degree interdependent. With the
poplar/Melampsora pathosystem, a direct influence of a climate
that is milder than the native one may favour an evergreen habit. But
the indirect influence, through the effect of the same climate on the
pathogen, is likely to militate against that shift. Often, however, the
evolutionary pressures from climatic and biotic factors would be
mutually reinforcing, as in the Medicago case.
In calling for a broad evaluation of biotic factors as evolutionary
drivers (or co-drivers) of plant phenology, the coverage is preliminary
and selective, representing an alert to the topic. Even a more
systematic literature review would still require interpretation of
individual cases. Challenges certainly exist in such evaluation. To
identify likely cases of biotic drivers, we consider it appropriate to
look largely to those who are closely familiar with individual plant
species and their ecology. Then detailed review and analysis of
available evidence is needed, but interpretation in individual cases may
still be problematic. From there, the general postulate of biotic
influences will need to be carried forward into hypotheses that are
observationally or experimentally testable. While woody perennials have
provided tantalising case histories, they can also pose major logistical
challenges in testing hypotheses.