Data Accessibility:
No new data were generated. Code needed to reproduce results of the
manuscript are available at
https://github.com/em-bellis/StrigaMacroecologyMS
Abstract:
Fitness responses to environment can shape species distributions, though
opposing eco-evolutionary processes can obscure environmental effects.
For example, host specificity influences parasite dynamics, but is
unclear how specialization of individual parasites or populations scales
up to continental distributions. Here, we develop a macroecological
framework to determine how host community structure affects
continent-scale specialization in Striga hermonthica, an African
parasitic plant of cereal crops. We find regional abundance of hosts in
cultivated cereal communities is associated with parasite specialization
observed in experiments. Moreover, abiotic environment at location of
origin predicts parasite performance on pearl millet and sorghum but not
maize, possibly due to the shorter coevolutionary history for maize andStriga . Our study demonstrates that patterns of parasite local
adaptation to host communities can emerge at continental scales and that
differential environmental tolerances of hosts indirectly shape the
distribution of specialist and generalist parasites.
Introduction:
Two central questions in biology are what maintains diversity in
environmental responses within species and what determines the
distribution of organisms across environmental gradients? These two
questions are intimately related but often studied separately. A common
hypothesis is that adaptation by populations to different local
environments is a major source of diversity in environmental responses
within species (Clausen et al. 1940; Kawecki & Ebert 2004).
Local adaptation is driven by genetic variation in fitness responses to
environment (“environmental preferences”) and thus local adaptation
may shape abundance patterns across environments. It is often
hypothesized that a species’ relative abundance in different habitats
reflects environmental preferences, but there are many empirical studies
where additional processes (e.g. dispersal limitation, Pulliam
1988) obscure or counteract environmental effects.
Local adaptation is defined as a genotype-by-environment interaction for
fitness such that home genotypes have higher fitness than foreign
genotypes (Kawecki & Ebert 2004). Local adaptation is common but not
ubiquitous, and often not detected in experiments (Leimu & Fischer
2008; Hereford 2009; Koskella 2014). The scale of environmental
heterogeneity relative to gene flow is one factor determining whether
populations adapt to local conditions, evolve generalist strategies
(Slatkin 1973; Penczykowski et al. 2016), or specialize on a
single environment (Brown & Pavlovic 1992). For example, local
adaptation is favored when the size of habitat patches is larger than
the characteristic scale of gene flow, while smaller habitat patches may
favor adaptation to the average of environments encountered, due to the
unpredictability of environments inhabited by offspring (Slatkin 1973;
Fig. 1). This pattern is readily apparent from empirical studies of
host-parasite metapopulations, where the scale of parasite adaptation to
local host genotypes depends strongly on habitat configuration and
relative scales of gene flow (Thrall & Burdon 1997; Thrall et
al. 2002; Laine 2005; Koskella et al. 2011; Tack et al.2014). However, it is unclear how local adaptation in metapopulations
scales up to determine species distribution and abundance (Petersonet al. 2019).
A simple hypothesis about distributions is that population size is
greatest where environmental conditions are most favorable (Brown 1984;
Fig. 1). Yet organisms are often excluded from ideal environments by
negative biotic interactions such as competition or predation (Buckley
& Roughgarden 2005). Organisms can also persistently occur in poor
environments due to immigration (i.e. source-sink dynamics, Pulliam
1988). Similarly, high extinction rates of parasite populations followed
by recolonization, or high adaptability of hosts, can also limit
parasite adaptation to their local hosts (Kaltz & Shykoff 1998). As a
result, recent studies have questioned the assumption underlying many
macroecological studies that patterns of environmental distribution
reflect individual fitness responses to environment (Osorio-Olveraet al. 2019; Holt 2020). Relatedly, parasite fitness may not
always be highest in environments where they are most abundant, though
several studies suggest parasite abundance is greater on preferred hosts
(Krasnov et al. 2004; Poulin 2005). Higher abundance may
translate to higher frequencies of parasite occurrence across sampled
localities (Poulin et al. 2012), but this trend is rarely linked
to patterns of local adaptation.
To address macroecological hypotheses of resource specialization,
parasite systems are perhaps some of the most promising (Stephenset al. 2016). For example, the growing availability of
host-parasite occurrence data has enabled continent-scale investigations
of host specificity (Fecchio et al. 2019; Wells et al.2019), defined as the number or diversity of hosts a parasite can infect
(Wells & Clark 2019). In contrast, host specialization (in the
Grinnellian sense) refers to variance in species’ performance across a
range of environments (Futuyma & Moreno 1988; Devictor et al.2010). Compared to host specificity (Fecchio et al. 2019),
macroecological studies of host specialization are scarce, perhaps due
to the need for quantitative measures of parasite performance which are
generally more difficult to obtain than occurrence data.
Here, we investigate continent-scale patterns of host specialization in
the parasitic plant Striga hermonthica. S. hermonthica is
widespread across diverse abiotic environments in East and West Africa
where it parasitizes grasses including the staple crops maize, pearl
millet, and sorghum and is a major constraint to food security (Runo &
Kuria 2018). Compared to pearl millet (Pennisetum glaucum ) and
sorghum (Sorghum bicolor ), which both have centers of
domestication in Africa, maize is a relatively recent host and has few
natural resistances to Striga (Rich & Ejeta 2008; Timko et
al. 2012). Hosts are characterized by mating systems from highly
outcrossing (pearl millet and maize) to predominately selfing (sorghum)
and a diversity of abiotic requirements. Unlike many microbial pathogens
and endoparasites, parasite generation times are similar to their hosts
(~1 year) leading to more balanced coevolutionary
dynamics. Parasitic plants are also large and conspicuous, so excellent
occurrence data are available from natural history collections. Host
specialized as well as generalist populations are known (Parker & Reid
1979). However, the eco-evolutionary determinants of specialization are
poorly characterized, despite detailed knowledge at the molecular level
on parasitic plant response to different hosts (Honaas et al.2013; Johnson et al. 2019; Lopez et al. 2019).
We synthesize previous experiments on host specialization, combined with
continental scale host and parasite distribution data, to ask three
questions: Q1) Does regional abundance of a host crop lead to local
specialization by parasites?, Q2) Is host specialization associated with
patterns of parasite occurrence on different hosts?, and Q3) Do abiotic
environmental gradients shape the distribution of specialist and
generalist parasites, suggesting that future dynamics of specialization
vs. generalization may be predicted by abiotic change?
Materials and
Methods: