Kin recognition, multilevel selection and altruism in crop sustainability

Transcription

1 Journal of Ecology 2017, 105, doi: / MINI-REVIEW: ECOLOGICAL SOLUTIONS TO GLOBAL FOOD SECURITY Kin recognition, multilevel selection and altruism in crop sustainability Guillermo P. Murphy 1, Clarence J. Swanton 1, Rene C. Van Acker 1 and Susan A. Dudley*,2 1 Department of Plant Agriculture, University of Guelph, 50 Stone Road East, Guelph, ON N1G 2W1, Canada; and 2 Department of Biology, McMaster University, 1280 Main Street West, Hamilton, ON L8K 4K1, Canada Summary 1. Intraspecific competition among crop plants is undesirable. Less competitive crops are predicted to increase yield and decrease the need for added resources. 2. Wild plants demonstrate the ability to recognize kin and potentially help their relatives by reducing their competitive behaviours, a form of altruism. Altruism can also evolve through multilevel selection. Are these processes relevant to sustainable agriculture? 3. Crops do grow predictably with kin. However, their evolution is more strongly dictated by artificial selection (crop breeding), which incorporates individual and group selection, making multilevel selection more relevant than kin selection in favouring altruism. While current crop breeding protocols attempt to target the reduction of competitive traits, early mass selection may have the opposite effect. 4. We predict that kin recognition itself is not relevant to crops, because of the consistently high relatedness within crop stands. Nonetheless, crops have shown cultivar and kin recognition. We argue that these responses cannot be assumed to demonstrate altruism, as current breeding practices offer little opportunity for kin selection. 5. Synthesis. There is the opportunity to favour altruism through artificial breeding. Here we suggest how crop breeding protocols could be changed to favour cooperation by increasing group selection during early breeding. Key-words: altruism, competition, cooperation, crop breeding, cultivar recognition, group selection, identity recognition, kin selection, multilevel selection, yield Introduction Intraspecific competition among crop plants is undesirable, because less competitive crops have increased stand yield (Donald 1968; Weiner et al. 2010). However, competitive behaviours increase individual fitness, while not competing is costly for an individual. Thus, stand performance cannot be predicted from individual plant performance (Hamilton 1964; Messmer et al. 2015). The ideotype approach to crop breeding indicates that more competitive individuals have higher individual performance at the cost of stand performance, while altruistic, non-competitive traits maximize stand performance (Donald 1968). The potential increase in stand performance from less competition and more altruism (File, Murphy & Dudley 2012) will benefit crop breeders and farmers. Breeding less competitive crops could lead to better *Correspondence author. sdudley@mcmaster.ca stand performance in high densities without increasing inputs of fertilizer and water (Dudley 2015). Growing plants in high densities could allow farmers to better use current farmland, one component of sustainability (Pretty 2008). However, breeding altruistic crops requires understanding the evolution of social behaviours in wild plants and crops. Here we review the evolution of social behaviour in plants and highlight how the crop breeding process could be altered to favour cooperation and altruism for future sustainable practices. Helping, cooperation and altruism Helping behaviours by one individual increase the fitness of another individual. We define cooperation as withinspecies helping that is not costly to the helper or increases the fitness of the helper, while altruism is costly helping 2017 The Authors. Journal of Ecology 2017 British Ecological Society

2 Altruism and crop sustainability 931 (Dudley 2015). While cooperation among plants may occur through many mechanisms (Dudley 2015), here we focus on how plants may potentially help one another by not expressing competitive behaviours, i.e. phenotypic plasticity to the presence of neighbours (Cahill & McNickle 2011). Altruism can be favoured by two different processes within plant populations: multilevel selection and kin selection. Both types of selection are created by the social environment. Plants typically interact competitively with their nearest neighbours (Milbau et al. 2007). Population structure, i.e., local groups within the larger population, creates an opportunity for multilevel selection on group vs. individual fitness (Fletcher & Zwick 2007). Relatedness among neighbours, i.e., whether neighbours of same species are relatives or unrelated strangers, provides the opportunity for kin selection on altruism (Hamilton 1964). MULTILEVEL SELECTION Being competitive increases individual fitness within a group, as appropriating resources before neighbours benefits the individual (Dudley, Murphy & File 2013). However, highly competitive groups may have reduced fitness, because of the costs of competition or luxury consumption of resources (Gersani et al. 2001; de Mazancourt & Schwartz 2012). Within the larger population, selection on competitiveness is the outcome of selection within subgroups for increased competitiveness vs. selection among subgroups for reduced competitiveness (Fig. 1). For example, height is a competitive trait and stem elongation is a competitive behaviour. Taller plants receive more sun and shade their neighbours. However, taller groups of plants are susceptible to lodging and allocate more biomass to stems, potentially reducing their average fitness (Pierik & de Wit 2014). Empirical multilevel selection studies in wild plants (reviewed in File, Murphy & Dudley 2012) show individual selection favouring increased height or elongation and group selection favouring reduced height or elongation. In crops, breeders have improved stand performance with dwarf varieties that do not elongate in the presence of competitors (Reynolds et al. 1994; Richards 2000). KIN SELECTION AND KIN RECOGNITION Kin selection can also favour altruism (see Appendix S1, Supporting Information). Kin selection theory extends the concept of fitness to include the effect of traits on the fitness of relatives who share genes (Hamilton 1964). Traits that help relatives can evolve through kin selection as long as the benefit to the relative, weighted by its relatedness, is greater than the cost to the individual displaying the trait (Hamilton 1964). Within natural plant populations where neighbours are not predictably related because seeds disperse stochastically, kin recognition provides a mechanism for an individual to direct help preferentially towards relatives, reducing the cost of altruism. Individual fitness (a) Individual selection (c) Parent selection Several plant species discriminate between siblings and strangers of the same species, with several plant functional traits demonstrating plasticity to the relatedness of neighbours (Chen, During & Anten 2012; Depuydt 2014). Kin recognition has been found in morphological, allocation, and leaf and root placement traits hypothesized to affect competitive ability (Dudley, Murphy & File 2013). These responses are species- and ecology-specific; growth with strangers increases above-ground competitive traits in light-limited environments, and below-ground competitive traits in nutrient-limited environments (Dudley & File 2007; Murphy & Dudley 2009). Cues of relatedness most often arise from root exudates (Semchenko, Saar & Lepik 2014), although aboveground volatiles are implicated in sagebrush (Karban et al. 2013) and light in Arabidopsis (Crepy & Casal 2014; though see Till-Bottraud & Villemereuil 2015). The growing body of research on plant identity recognition also includes species and self/non-self recognition (Chen, During & Anten 2012; Depuydt 2014). Altruism and crops MULTILEVEL SELECTION Helping trait (b) Group selection (d) Offspring response Fig. 1. Multilevel selection on an altruistic trait, e.g. not increasing competitive ability with neighbours. In this scenario, groups with more helping have higher fitness; however, helping others is costly to the individual, resulting in a negative relationship between helping and fitness within a group. Ovals correspond to single population associations of trait and fitness, with the shaded area indicating breeder selection. Selection by a breeder on individual performance (a) favours low levels of helping. Selection by a breeder on group performance (b) favours increased helping. Selecting the highest performers from the highest performing group (c) favours helping (d), but to a lesser extent than group selection alone (b). How are multilevel selection and kin selection relevant to the evolution of altruism in crops? The answer depends on how crops evolve. Crops do not evolve during crop production in

3 932 G. P. Murphy et al. farm fields. Crops evolve during artificial selection (breeding), which includes a changing social structure and changing levels of selection. Typical phenotypic selection in an inbreeding crop (Fig. 2 left) follows a pattern of early individual selection (mass selection), later mixed individual and group selection, and finally group selection (progeny row selection). This process creates multilevel selection (Goodnight 1985), with group selection for the best performing progeny rows, and mass selection for the best performing individuals from these rows. Early mass selection selects against altruism, as competitive individuals are more vigorous than altruistic neighbours (Fig. 1a). Mixed individual and group selection (Fig. 1c,d) favours altruism less than group selection alone (Fig. 1b). We predict that group selection throughout breeding should favour altruism (Figs 1b and 2 right). An empirical selection experiment (Goodnight 1985) on Arabidopsis performance, measured as plant leaf area, supports this prediction. Both individual and group selection for reduced leaf area resulted in the evolution of plants with less leaf area, as expected. In contrast, when selection was for increased leaf area, group selection resulted in the expected evolution of greater leaf area, but surprisingly, individual selection resulted in the evolution of reduced leaf area. This experiment demonstrates antagonism between individual and group performance and the benefits of group selection. IDENTITY RECOGNITION AND CROPS While selection imposed during crop breeding can disfavour or favour altruism, it is occurring in uniformly highly related populations. Consequently, there is no opportunity for selection on kin recognition. Nonetheless, crops demonstrate cultivar recognition as well as species recognition. Most kin recognition studies in crops measured same vs. different cultivar recognition (Fang et al. 2011, 2013; Zhu & Zhang 2013; Murphy et al. 2017). Only one study considered kin recognition between maternal sibships, paralleling wild plant studies (Zhang et al. 2016). In rice, soybean and maize (Fang et al. 2011, 2013), roots of more related plants were shown to readily intergrow while roots of less related plants avoided roots of neighbours. In a modern wheat cultivar, root allocation increased in response to growing with plants of a different cultivar, though the older cultivar did not respond (Zhu & Zhang 2013). In soybean, three cultivars did not differ in biomass allocation when grown with other soybean cultivars (Glycine max). However, allocation towards leaves increased when soybean cultivars grew with neighbours of an ancestral soybean species (Glycine soja) or with neighbours of a different genus of crop legume (Phaseolus vulgaris), demonstrating species recognition (Murphy et al. 2017). Zhang et al. (2016) measured kin recognition in nitrogen acquisition and biomass allocation traits for maternal sibships of sorghum and soybean. They found A B Parental A B F1 F2 F3 F4 Fn Fig. 2. Typical phenotypic selection for an inbreeding crop (left) vs. a group selection approach to breeding (right). In both, homozygous parental lines are crossed and the resulting heterozygous, genetically identical F1s are allowed to self. In the typical programme, mass selection (phenotypic selection on individuals) starts in the genetically variable F2 generation. The F2s are grown in bulk plots, and individual plants with desirable traits and high performance are selected as parents for the F3 generation. With only two parental lines, the bulk plots are predictably highly related. In the later generations, yield tests are done in progeny rows: each row is a half- or full-sib family grown in crop production conditions. In this example, in the F3 generation, the highest performing plants from the highest performing progeny rows are selected. Future generations may involve selection of high-performing progeny rows. Redrawn from (Messmer et al. 2015, page 29 left). The group selection approach (right) is similar to the typical one, except that population structure is created in the F2 generation, and all members of high-performing groups are selected for the next generation.

4 Altruism and crop sustainability 933 differing responses to same-species strangers in these crops: sorghum increased root allocation and soybean increased N uptake and the proportion of nitrogen from nitrate. Taken together, these studies indicate that identity recognition systems are present in crop plants despite high stand relatedness during breeding. Plasticity to the relatedness of neighbours indicates the ability to recognize identity by crops. However, cultivars are derived from widely separated wild populations, and then grown in pure stands. Consequently, there is less reason to interpret the kin/stranger or same/different cultivar recognition responses as altruistic vs. competitive. As these crop studies use few cultivars, differences among cultivars in overall competitiveness or allelopathy could explain same vs. different cultivar responses. Not all traits are adaptive, and alternative hypotheses for the presence of cultivar and kin recognition include vestiges of ancestral competitive responses, the consequence of selection on correlated traits or genetic drift in traits no longer under selection. One intriguing possibility is a correlated response to species recognition (Murphy et al. 2017), as crops often compete with weeds. Concluding remarks Breeding for altruistic and competitive traits could improve sustainability. Plants sense neighbours and respond by preempting resources before neighbours access them (de Mazancourt & Schwartz 2012). This overconsumption requires excess resources and cues a more competitive phenotype at the cost of future yield, resulting in a tragedy of the commons (Gersani et al. 2001). However, changes to crop breeding protocols (Fig. 2 right) could favour altruism by introducing population structure (e.g. as in animal breeding, Muir 1996) during early mass selection. Population structure would provide an opportunity for selection on indiscriminate altruism and result in group selection that could favour altruism. Though kin recognition is not relevant to crops, because the consistently high relatedness within crop stands does not provide any function for kin recognition, other kinds of identity recognition could be important for crop performance. Same vs. different species recognition could help plants better compete with weeds while self vs. no-self recognition could reduce within-plant competition. Kin recognition responses in wild crop relatives could inform breeders on potential competitive, cooperative and altruistic traits. Authors contributions S.A.D., G.P.M., C.S. and R.V.A. conceived the ideas; S.A.D. and G.P.M. led the writing of the manuscript. All authors contributed critically to the draft and gave final approval for publication. Acknowledgements Financial support for this work was provided by the Natural Science and Engineering Research Council of Canada (NSERC) through Discovery Grants to C.J.S. and S.A.D. The authors thank Lewis Lukens and Peter Pauls for helpful discussion. The authors have no conflicts of interest. Data accessibility This paper does not use data. References Cahill, J.F. & McNickle, G.G. (2011) The behavioral ecology of nutrient foraging by plants. Annual Review of Ecology, Evolution, and Systematics, 42, Chen, B.J.W., During, H.J. & Anten, N.P.R. (2012) Detect thy neighbor: identity recognition at the root level in plants. Plant Science, 195, Crepy, M. & Casal, J.J. (2014) Photoreceptor-mediated kin recognition in plants. New Phytologist, 205, Depuydt, S. (2014) Arguments for and against self and non-self root recognition in plants. Frontiers in Plant Science, 5, 614. Donald, C.M. (1968) The breeding of crop ideotypes. Euphytica, 17, Dudley, S.A. (2015) Plant cooperation. 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