Here, we reply to the stimulating comments from Sagoff [1] and Rossberg [2] on Segar et al. [3]

Fayle, TM

Kitching, RL

Lewinsohn, TM

Lewis, OT

Maunsell, SC

Novotny, V

Segar, ST

Srivastava, DS

Trends in Ecology & Evolution

Segar, S.T.

Fayle, T.M.

Srivastava, D.S.

Lewinsohn, T.M.

Lewis, O.T.

Novotny, V.

Kitching, R.L.

Maunsell, S.C.

Harper Adams University Repository

Segar, S.T., Fayle, T.M., Srivastava, D.S., Lewinsohn. T.M., Lewis, O.T., Novotny, V., Kitching, R.L. and Maunsell, S.C. 2020. On the perils of ignoring evolution in networks.  Trends in Ecology & Evolution. 24 August 2020 On the perils of ignoring evolution in networks  by Segar, S.T., Fayle, T.M., Srivastava, D.S., Lewinsohn. T.M., Lewis, O.T., Novotny, V., Kitching, R.L. and Maunsell, S.C.  Copyright, publisher and additional Information: This is the author accepted manuscript. The final published version (version of record) is available online via Elsevier. This version is made available under the CC-BY-ND-NC licence Please refer to any applicable terms of use of the publisher DOI link to the version of record on the publisher’s website     On the Perils of Ignoring Evolution in Networks  Simon T. Segar1,2,3*, Tom M. Fayle1,2,4, Diane S. Srivastava5, Thomas M. Lewinsohn6,7, Owen T. Lewis8, Vojtech Novotny,1,2, Roger L. Kitching9, Sarah C. Maunsell10 1 Biology Centre, Czech Academy of Sciences, Institute of Entomology, Branisovska 1760, 5 370 05 Ceske Budejovice, Czech Republic,  2 University of South Bohemia in Ceske Budejovice, Faculty of Science, Branisovska 1760, 370 05 Ceske Budejovice, Czech Republic,  3 Department of Crop and Environment Sciences, Harper Adams University, Newport, Shropshire, TF10 8NB, UK 10 4 Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah, Kota Kinabalu, Sabah, Malaysia,  5 Dept of Zoology & Biodiversity Research Centre, University of British Columbia 6270 University Blvd Vancouver BC Canada V6T 1Z4,  6 Depto Biologia Animal, Instituto de Biologia, University of Campinas, Campinas 13083-15 870, São Paulo, Brazil,  7 Wissenschaftskolleg zu Berlin, Berlin 14193, Germany,  8 Department of Zoology, South Parks Road, Oxford, OX1 3PS, UK,  9 Environmental Futures Research Institute, Griffith University, Brisbane, Queensland 4111, Australia 20 10 Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, 02138, USA  Corresponding author: ssegar@harper-adams.ac.uk (Simon T. Segar) Twitter Handle: @simonsegar 25 Address: Department of Crop and Environment Sciences, Harper Adams University, Newport, Shropshire, TF10 8NB Telephone: +441952815478    30      35 Here we reply to the stimulating comments from Sagoff [1] and Rossberg [2] on Segar et al. [3]. Sagoff posits that species assemblages are largely fortuitous and ephemeral, which thwarts opportunities for coevolutionary processes [4]. Given the dynamic nature of ecological communities, have populations from different interacting species had sufficient time in which to generate selective pressure on each other? As Rossberg points out, in long-lasting and highly 40 intimate bipartite networks, “frequent co-occurrence of the two taxa” is required for evolutionary lockstep between v (vulnerability) and f (foraging) traits. Fitness “seascapes” [2] stem from constant community turnover: but the adaptive troughs and peaks of the shifting seascape can persist and allow reciprocal evolutionary change if allelic turnover is rapid and selection strong enough. How do we specify “frequent co-occurrence”? Since Janzen’s 1985 45 appraisal of coevolution [4], Colpoda protozoans have been through over 53,000 generations: resistance to mosquito predators develops in 50 [5]. We do agree that ecological (non-genetic) fitting is widespread. However, biotic selection within ecological networks does occur, is detectable, and its effects are far from trivial. Empirical support 50 Research across a range of systems has demonstrated that microevolutionary change can occur over ecological time scales as populations from different species interact, creating eco-evolutionary feedback loops [6]. In guppies, phenotypic responses to predation intensity, likely with a genetic basis, can occur in a matter of years and the resultant divergence in guppy feeding preferences alters the structure of invertebrate assemblages and local stream food webs 55 [7]. Indeed, the most convincing evidence for the role of evolution in networks is empirical. Loci under selection vary when more than one species is involved: for example, selection for resistance to deer in ivy leaf morning glory, Ipomoea hederacea, is stronger when plants are also under attack by insects [8]. The probability and strength of such interactions are in part 60 determined by network structure. Ecological context is key, both past and present. Without invoking group selection, there is ample evidence that multiple interactants can act in concert to produce non-additive selective pressures that influence network structure. For example, multiple inter-individual interactions [3] engender diffuse coevolution [9]. It is now widely accepted that selective pressure originates from multiple sources [10] and that various 65 combinations of abiotic and biotic drivers act to shape phenotypic divergence.  It is also apparent that populations from different interacting species do generate selective pressure on each other and co-occurrence durations are sufficiently long for evolution to occur. This assertion is substantiated by the local adaptations of widespread mutualists (the ‘co-evolutionary mosaic’) [11]. We do recognize that the persistence of such interactions is likely 70 to vary greatly, and accordingly affect the strength of selective pressure. Biotic selection may or may not lead to coevolution and subsequent co-speciation, but it can certainly determine key parameters such as host use and resistance. Wallace’s line and Darwin’s bridge Biotic selection can also determine character displacement of phenotypes within interbreeding 75 populations and subsequent divergence into non-interbreeding populations (i.e. speciation). Such phenotypic divergence can be traced across phylogenies (macroevolution). In other words, we must look to Wallace as well as Darwin. Wallace recognised the combined role of evolutionary and geological processes in determining the distinct clustering of Earth’s biodiversity across geographic regions - the regional species pool from which local networks 80 are drawn [12]. Descent with modification has shaped the traits through which populations interact upon first encounter [2], even if the interacting populations did not evolve together. Phylogenetic signal in interactions can therefore determine network structure [2]. We agree with Sagoff  [1]  that evolutionary processes such as speciation, and spatial ones such as dispersal, are important co-determinants of the species pool from which networks are 85 assembled. Sagoff focuses his critique on microevolution, but the macroevolutionary processes determining the generation of species diversity should not be undervalued. As expounded by Reznick and Ricklefs [13], Darwin’s theory of evolution spans microevolution and macroevolution. Individuals within a species can diverge, with some lineages going extinct, while reproductive barriers build up between others. Biotic interactions are key components of 90 the adaptive landscape and speciation process. For example, speciation through ecological divergence and evolutionary novelty is common in adaptive radiations. There appears to be consensus that speciation is of importance in determining the composition of ecological networks. Dispersal is crucial for eco-evolution: it determines population densities and mediates gene flow, trait mixing and local adaptation. Darwin recognised that dispersal 95 contributes as much as the biotic environment in determining species distributions. We consider these processes concurrently, hence allowing the data to gauge the role of evolution in networks. Invasion and natural laboratories Sagoff [1] claims that novel and “heirloom” ecosystems do not differ. On the contrary, 100 widespread invasions have repeatedly demonstrated that networks can be rendered novel, simplified and “rewired” following either the introduction of pre-adapted species with which they have not evolved, or human-induced extinction of native species [14,15]. Take invasions on islands, for example. Further, human-mediated species invasions have led to the biotic homogenization of Earth, reducing the potential for demographic or evolutionary rescue. 105 Selection for traits that raise the likelihood of successful invasion may take place in the native range, so that evolutionary history can be an effective predictor of network persistence. Evolution can be rapid in trophic interactions and occur more broadly across communities [6] with no requirement for long-term phylogenetic associations. To conclude, Rossberg’s [2] formalisations and models provide a welcome path for further 110 insights into our questions. Sagoff [1] seems to impose a stark choice between either a Gleasonian world in which species are independent in traits and distributions, co-occurrences are entirely fortuitous and interactions are of no evolutionary consequence, or a naïve pan-evolutionary world which is entirely structured by simple pairwise coevolutionary processes. Our proposed framework [3] fits neither oversimplified extreme: we seek a richer, more 115 realistic and more fruitful combination of theory and documented network features in order to advance our understanding of how these come to be, are maintained and can be modified. We ignore evolution in ecological networks at our peril.   120      125      130     References 135 1  Sagoff, M. (2020) Ecological Networks: Response to Segar et al. Trends Ecol. Evol. DOI: 10.1016/j.tree.2020.04.008 2  Rossberg, A.G. (2020) What Are the Fundamental Questions Regarding Evolution in Ecological Networks? Trends Ecol. Evol. DOI: 10.1016/j.tree.2020.06.004 3  Segar, S.T. et al. (2020) The Role of Evolution in Shaping Ecological Networks. Trends 140 Ecol. Evol. 35, 454–466 4  Janzen, D.H. (1985) On Ecological Fitting. Oikos 45, 308–310 5  terHorst, C.P. et al. (2010) Evolution of prey in ecological time reduces the effect size of predators in experimental microcosms. Ecology 91, 629–636 6  Koch, H. et al. (2014) Why rapid, adaptive evolution matters for community dynamics. 145 Front. Ecol. Evol. 2,  7  Bassar, R.D. et al. (2010) Local adaptation in Trinidadian guppies alters ecosystem processes. Proc. Natl. Acad. Sci. USA 107, 3616–3621 8  Stinchcombe, J.R. and Rausher, M.D. (2001) Diffuse Selection on Resistance to Deer Herbivory in the Ivyleaf Morning Glory, Ipomoea hederacea. Am. Nat. 158, 376–388 150 9  Janzen, D.H. (1980) When is it coevolution? Evolution 34, 611–612 10  Palacio, F.X. et al. (2020) Selection on fruit traits is mediated by the interplay between frugivorous birds, fruit flies, parasitoid wasps and seed-dispersing ants. J. Evol. Biol. 33, 874–886 11  Anderson, B. and Johnson, S.D. (2007) The geographical mosaic of coevolution in a 155 plant-pollinator mutualism: coevolution between mutualists. Evolution 62, 220–225 12  Wallace, A. (1876) The Geographical Distribution of Animals, 1876. Hafner, New York  13  Reznick, D.N. and Ricklefs, R.E. (2009) Darwin’s bridge between microevolution and macroevolution. Nature 457, 837–842 14  Mathiasson, M.E. and Rehan, S.M. (2020) Wild bee declines linked to plant-pollinator 160 network changes and plant species introductions. Insect Cons. Div. In Press,  15  Simberloff, D. (2005) Non-native Species DO Threaten the Natural Environment! J. Agr. Environ. Ethic. 18, 595–607  

On the perils of ignoring evolution in networks

Segar, Simon T

Fayle, Tom M

Srivastava, Diane S

Lewinsohn, Thomas M

Lewis, Owen T

Novotny, Vojtech

Kitching, Roger L

Maunsell, Sarah C

Oxford University Research Archive

On the perils of ignoring evolution in networks  Simon T. Segar1,2,3*, Tom M. Fayle1,2,4, Diane S. Srivastava5, Thomas M. Lewinsohn6,7, Owen T. Lewis8, Vojtech Novotny,1,2, Roger L. Kitching9, Sarah C. Maunsell10 1 Biology Centre, Czech Academy of Sciences, Institute of Entomology, Branisovska 1760, 5 370 05 Ceske Budejovice, Czech Republic,  2 University of South Bohemia in Ceske Budejovice, Faculty of Science, Branisovska 1760, 370 05 Ceske Budejovice, Czech Republic,  3 Department of Crop and Environment Sciences, Harper Adams University, Newport, Shropshire, TF10 8NB, UK 10 4 Institute for Tropical Biology and Conservation, Universiti Malaysia Sabah, Kota Kinabalu, Sabah, Malaysia,  5 Dept of Zoology & Biodiversity Research Centre, University of British Columbia 6270 University Blvd Vancouver BC Canada V6T 1Z4,  6 Depto Biologia Animal, Instituto de Biologia, University of Campinas, Campinas 13083-15 870, São Paulo, Brazil,  7 Wissenschaftskolleg zu Berlin, Berlin 14193, Germany,  8 Department of Zoology, South Parks Road, Oxford, OX1 3PS, UK,  9 Environmental Futures Research Institute, Griffith University, Brisbane, Queensland 4111, Australia 20 10 Department of Organismic and Evolutionary Biology, Harvard University, Cambridge, MA, 02138, USA  Corresponding author: ssegar@harper-adams.ac.uk (Simon T. Segar) Twitter Handle: @simonsegar 25 Address: Department of Crop and Environment Sciences, Harper Adams University, Newport, Shropshire, TF10 8NB Telephone: +441952815478    30      35  Here we reply to the stimulating comments from Sagoff [1] and Rossberg [2] on Segar et al. [3]. Sagoff posits that species assemblages are largely fortuitous and ephemeral, which thwarts opportunities for coevolutionary processes [4]. Given the dynamic nature of ecological communities, have populations from different interacting species had sufficient 40 time in which to generate selective pressure on each other? As Rossberg points out, in long-lasting and highly intimate bipartite networks, “frequent cooccurrence of the two taxa” is required for evolutionary lockstep between v (vulnerability) and f (foraging) traits. Fitness “seascapes” [2] stem from constant community turnover: but the adaptive troughs and peaks of the shifting seascape can persist and allow reciprocal evolutionary change if allelic 45 turnover is rapid and selection strong enough. How do we specify “frequent cooccurrence”? Since Janzen’s 1985 appraisal [4], bivoltine insects have been through 70 generations: resistance to parasitoids can develop in 14 generations [5]. We do agree that ecological (non-genetic) fitting is widespread. However, biotic selection within ecological networks does occur, is detectable, and its effects are far from trivial. 50 Empirical support Research across a range of systems has demonstrated that microevolutionary change can occur over ecological time scales as populations from different species interact, creating eco-evolutionary feedback loops [6], with parasites and pathogens providing some of the best examples. How is this relevant to ecological networks? In guppies phenotypic responses to 55 predation, likely with a genetic basis, can occur in a matter of years. Low and high-predation guppy phenotypes also diverge in their feeding preferences which alters the structure of invertebrate assemblages and local stream food webs [7]. Indeed, the most convincing evidence for the role of evolution in networks is empirical. Loci under selection vary when more than one species is involved: for example, selection for 60 resistance to deer in ivy leaf morning glory, Ipomoea hederacea, is stronger when plants are also under attack by insects [8]. The probability and strength of interactions are in part determined by network structure. Ecological context is key, both past and present. Without invoking group selection, there is ample evidence that multiple interactants can act in concert to produce non-additive selective pressure that will influence network structure: best 65 modelled as interindividual interactions [3] that can, in turn, engender diffuse coevolution [9]. Clearly, selective pressure originates from multiple sources [10]. That various combinations of abiotic and biotic drivers act to shape phenotypic divergence is widely accepted.  Populations from different interacting species do generate selective pressure on each other 70 and co-occurrence durations are sufficiently long for evolution to occur. This is clear from local adaptations of widespread mutualists (the ‘co-evolutionary mosaic’) [11]. The persistence of such interactions is likely to vary greatly, and accordingly affect the strength of selective pressure. Biotic selection may or may not lead to coevolution and subsequent co-speciation, but it can certainly determine key parameters such as host use and resistance. 75 Wallace’s line and Darwin’s bridge Biotic selection can determine character displacement of phenotypes within interbreeding populations and subsequent divergence into non-interbreeding populations (i.e. speciation). Phenotypic divergence can be traced across phylogenies (macroevolution). In other words, we must look to Wallace as well as Darwin. Wallace recognised the combined role of 80 evolutionary and geological processes in determining the distinct clustering of Earth’s biodiversity across geographic regions - the regional species pool from which local networks are drawn [12]. Descent with modification has shaped the traits through which populations interact upon first encounter [2], even if the interacting populations did not evolve together. Phylogenetic signal in interactions can determine network structure [2]. 85 We agree with Sagoff [1]  that evolutionary processes such as speciation, and spatial ones such as dispersal, are important co-determinants of the species pool from which networks are assembled. Sagoff focuses his critique on microevolution, but the macroevolutionary processes determining the generation of species diversity should not be undervalued. As expounded by Reznick and Ricklefs [13], Darwin’s theory of evolution spans microevolution 90 and macroevolution. Individuals within a species can diverge, with some lineages going extinct, while reproductive barriers build up between others. Biotic interactions are key components of the adaptive landscape and speciation process. For example, speciation through ecological divergence and evolutionary novelty is common in adaptive radiations. There appears to be consensus that speciation is of importance in determining the 95 composition of ecological networks. Dispersal is key for eco-evolution: it determines population densities and mediates gene flow, trait mixing and local adaptation. Darwin recognised that dispersal contributes as much as the biotic environment in determining species distributions. We consider these processes concurrently, hence allowing the data to determine the role of evolution in networks. 100 Invasion and natural laboratories Sagoff [1] claims that novel and “heirloom” ecosystems do not differ. On the contrary, widespread invasions have repeatedly demonstrated that networks can be rendered novel, simplified and “rewired” following either the introduction of pre-adapted species with which they have not evolved, or human induced extinction of native species [14,15]. Further, 105 human-mediated species invasions have led to the biotic homogenization of Earth, reducing the potential for demographic or evolutionary rescue. Selection for traits that raise the likelihood of successful invasion may happen in the native range, so that evolutionary history can be an effective predictor of network persistence. Evolution can be rapid in trophic interactions and occur more broadly across communities [6] with no requirement for long-110 term phylogenetic associations. To conclude, Rossberg’s [2] formalisations and models provide a welcome path for further insights into our questions. Sagoff [1] seems to impose a stark choice between a Gleasonian world in which species are independent in traits and distributions, cooccurrences are entirely fortuitous and interactions are of no evolutionary consequence; and, a naïve pan-evolutionary 115 world which is entirely structured by simple pairwise coevolutionary processes. Our proposed framework [3] fits neither oversimplified extreme: we seek a richer, more realistic and more fruitful combination of theory and documented network features in order to advance our understanding of how these come to be, are maintained and modified. We ignore evolution in networks and communities at our peril. 120   References 1  Sagoff, M. (2020) Ecological Networks: Response to Segar et al. Trends Ecol. Evol. DOI: 10.1016/j.tree.2020.04.008 125 2  Rossberg, A.G. (2020) What Are the Fundamental Questions Regarding Evolution in Ecological Networks? Trends Ecol. Evol. DOI: 10.1016/j.tree.2020.06.004 3  Segar, S.T. et al. (2020) The Role of Evolution in Shaping Ecological Networks. Trends Ecol. Evol. 35, 454–466 4  Janzen, D.H. (1985) On Ecological Fitting. Oikos 45, 308–310 130 5  Tomasetto, F. et al. (2017) Intensified agriculture favors evolved resistance to biological control. Proc. Natl. Acad. Sci. USA 114, 3885–3890 6  Koch, H. et al. (2014) Why rapid, adaptive evolution matters for community dynamics. Front. Ecol. Evol. 2,  7  Bassar, R.D. et al. (2010) Local adaptation in Trinidadian guppies alters ecosystem 135 processes. Proc. Natl. Acad. Sci. USA 107, 3616–3621 8  Stinchcombe, J.R. and Rausher, M.D. (2001) Diffuse Selection on Resistance to Deer Herbivory in the Ivyleaf Morning Glory, Ipomoea hederacea. Am. Nat. 158, 376–388 9  Janzen, D.H. (1980) When is it coevolution? Evolution 34, 611–612 10  Palacio, F.X. et al. (2020) Selection on fruit traits is mediated by the interplay between 140 frugivorous birds, fruit flies, parasitoid wasps and seed-dispersing ants. J. Evol. Biol. 33, 874–886 11  Anderson, B. and Johnson, S.D. (2007) The geographical mosaic of coevolution in a plant-pollinator mutualism: coevolution between mutualists. Evolution 62, 220–225 12  Wallace, A. (1876) The Geographical Distribution of Animals, 1876. Hafner, New York  145 13  Reznick, D.N. and Ricklefs, R.E. (2009) Darwin’s bridge between microevolution and macroevolution. Nature 457, 837–842 14  Mathiasson, M.E. and Rehan, S.M. (2020) Wild bee declines linked to plant-pollinator network changes and plant species introductions. Insect Cons. Div. n/a,  15  Simberloff, D. (2005) Non-native Species DO Threaten the Natural Environment! 150 Journal of Agricultural and Environmental Ethics 18, 595–607  

English

Here, we reply to the stimulating comments from Sagoff [ 1 ] and Rossberg [ 2 ] on Segar et al. [ 3 ]. Sagoff posits that species assemblages are largely fortuitous and ephemeral, which thwarts opportunities for coevolutionary processes [ 4 ]. Given the dynamic nature of ecological communities, have populations from different interacting species had sufficient time in which to generate selective pressure on each other? As Rossberg points out, in long-lasting and highly intimate bipartite networks, ‘frequent co-occurrence of the two taxa’ is required for evolutionary lockstep between vulnerability (v) and foraging (f) traits. Fitness ‘seascapes’ [ 2 ] stem from constant community turnover: but the adaptive troughs and peaks of the shifting seascape can persist and allow reciprocal evolutionary change if allelic turnover is rapid and selection strong enough. How do we specify ‘frequent co-occurrence’? Since Janzen’s 1985 appraisal of coevolution [ 4 ], Colpoda protozoans have been through over 53 000 generations: resistance to mosquito predators develops in 50 [ 5 ]. We do agree that ecological (nongenetic) fitting is widespread. However, biotic selection within ecological networks does occur, is detectable, and its effects are far from trivial.Full Tex

Griffith Research Online

On the Perils of Ignoring Evolution in Networks (Letter)

ORA - Oxford University Research Archive

https://hau.repository.guildhe.ac.uk/id/eprint/17585/1/Simon%20Segar%20on%20the%20perils%20upload.pdf

On the perils of ignoring evolution in networks

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