Statement of Authorship:
ESB, CWD, and JRL conceived of the study. ESB designed geographic and
environmental analyses. CMM developed linear mixed models. ESB, CMM, and
JRL wrote the manuscript with input from CWD.
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 adaptation of parasites to local host communities may scale up to continental distributions. Here, we develop a macroecological framework to determine how host community structure affects the distribution of specialist and generalist populations of Striga hermonthica, an African parasitic plant of cereal crops. Combining data from global crop production and parasite experimental trials, we find that parasites perform best on the host species that is most common in their location of origin. Moreover, niche model contrasts predict parasite specialization on two hosts that evolved alongside Striga during domestication (pearl millet and sorghum), indicating that specialist parasites may be most likely to occur where host niches differ most in multivariate environmental space. 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. By predicting spatial dynamics of parasite specialization versus generalization directly from environmental data, our approach may help inform current and future management of pests and disease.
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 and Ebert 2004). Local adaptation is driven by genetic variation in fitness responses to the 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 such as dispersal (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 and Ebert 2004). Local adaptation is common but not ubiquitous (Leimu and Fischer 2008, Hereford 2009) and often difficult to detect in host-parasite systems because parasites may be better adapted to host populations from the recent past than to contemporary host populations (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 and 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). 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 and 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 (Peterson et al. 2019).
A simple hypothesis about distributions is that population size is greatest where environmental conditions are most favorable (Brown 1984). Yet organisms are often excluded from ideal environments by negative biotic interactions such as competition or predation (Buckley and Roughgarden 2005). Organisms can also persistently occur in poor environments due to immigration (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 and 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-Olvera et 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 (Stephens et 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 and Clark 2019). In contrast, host specialization (in the Grinnellian sense) refers to variance in species’ performance across a range of environments (Futuyma and 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. A root hemiparasite of the broomrape family (Orobanchaceae), S. hermonthica is characterized by a complex life cycle. Seeds can remain viable in soils for up to ~14 years (Bebawi et al. 1984) until germination, which requires detection of specific hormones (strigolactones) present in host root exudates (Cook et al. 1966). Other host-derived molecules trigger the formation of the haustorium (Cui et al. 2018), a specialized feeding structure used to invade host tissues and form vascular connections. Through these connections, parasitic plants suppress host immune responses (Shahid et al. 2018) and acquire water and nutrients to support their own development, emergence, and reproduction (Clarke et al. 2019). S. hermonthica is widespread across diverse abiotic environments in East and West Africa where it parasitizes grasses including maize, pearl millet, sorghum, sugarcane, and rice and is a major constraint to food security (Rodenburg et al. 2016, Runo and Kuria 2018). Compared to pearl millet (Pennisetum glaucum) and sorghum (Sorghum bicolor), which both have centers of domestication in Africa (Winchell et al. 2017, Burgarella et al. 2018), maize is a relatively recent host and has few natural resistances to Striga (Rich and Ejeta 2008, Timko et al. 2012).
Parasitic plants offer numerous advantages for studying the eco-evolutionary dynamics of parasitism. S. hermonthica 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. The potential for reciprocal coevolution (rather than asymmetrical adaptation of parasites to hosts often assumed in agricultural settings) is supported by a recent study of sorghum and S. hermonthica. Bellis et al. (2020) found evidence that S. hermonthica prevalence imposed spatially-varying selection on sorghum landraces, promoting among-population diversity in sorghum alleles for S. hermonthica resistance. Parasitic plants are large and conspicuous, so excellent occurrence data are available from natural history collections without a need for dissections or molecular diagnostics. Host specialized as well as generalist populations are known (Parker and 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 observed 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: