Urban areas are expanding worldwide, and have become a dominant part of the landscape for many species. Urbanization can fragment pre-existing populations of vulnerable species leading to population declines and the loss of connectivity. On the other hand, expansion of urban areas can also facilitate the spread of human commensals including pests. Knowledge of the features of cityscapes that facilitate gene flow and maintain diversity of pests is thus key to their management and eradication.
Cities are complex mosaics of natural and manmade surfaces, and habitat quality is not only influenced by physical aspects of the cityscape but also by socioeconomic factors and human behaviour. Constant development means that cities also change rapidly in time; contemporary urban life reflects only a snapshot of the environmental conditions faced by populations. It thus remains a challenge to identify the features that actually drive ecology and evolution of populations in cities [1]. While several studies have highlighted strong urban clines in genetic structure and adaption [2], few have considered the influence of factors beyond physical aspects of the cityscape or historical processes.
In this paper, Stragier et al. [3] sought to identify the current and past features of the cityscape and socioeconomic factors that shape genetic structure and diversity of the house mouse (Mus musculus domesticus) in Dakar, Senegal. The authors painstakingly digitized historical maps of Dakar from the time of European settlement in 1862 to present. The authors found that the main spatial genetic cline was best explained by historical cityscape features, with higher apparent gene flow and genetic diversity in areas that were connected earlier to initial European settlements. Beyond the main trend of spatial genetic structure, they found further evidence that current features of the cityscape were important. Specifically, areas with low vegetation and poor housing conditions were found to support large, genetically diverse populations. The authors demonstrate that their results are reproducible using several statistical approaches, including modeling that explicitly accounts for spatial autocorrelation.
The work of Stragier et al. [3] thus highlights that populations of city-dwelling species are the product of both past and present cityscapes. Going forward, urban evolutionary ecologists should consider that despite the potential for rapid evolution in urban landscapes, the signal of a species’ colonization can remain for generations.

References

[1] Rivkin, L. R., Santangelo, J. S., Alberti, M. et al. (2019). A roadmap for urban evolutionary ecology. Evolutionary Applications, 12(3), 384-398. doi: 10.1111/eva.12734
[2] Miles, L. S., Rivkin, L. R., Johnson, M. T., Munshi‐South, J. and Verrelli, B. C. (2019). Gene flow and genetic drift in urban environments. Molecular ecology, 28(18), 4138-4151. doi: 10.1111/mec.15221
[3] Stragier, C., Piry, S., Loiseau, A., Kane, M., Sow, A., Niang, Y., Diallo, M., Ndiaye, A., Gauthier, P., Borderon, M., Granjon, L., Brouat, C. and Berthier, K. (2020). Interplay between historical and current features of the cityscape in shaping the genetic structure of the house mouse (Mus musculus domesticus) in Dakar (Senegal, West Africa). bioRxiv, 557066, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/557066

Mammals show a very low level of variation in vertebral count, both among and within species, in comparison to other vertebrates [1]. Jordan’s rule for fishes states that the vertebral number among species increases with latitude, due to ambient temperatures during development [2]. Temperature has also been shown to influence vertebral count within species in fish [3], amphibians [4], and birds [5]. However, in mammals the count appears to be constrained, on the one hand, by a possible relationship between the development of the skeleton and the proliferations of cell lines with associated costs (neural malformations, cancer etc., [6]), and on the other by the cervical origin of the diaphragm [7].
Knight et al. [8] investigate the effect of intrauterine temperature variation on skeletal morphology during development, and focus on a particular mammal, Dasypus novemcinctus, or nine-banded armadillo. Armadillos (Xenarthra) and are characterized by relatively low body temperatures and low basal rates of metabolism. Dasypus novemcinctus is the only xenarthran mammal to have naturally expanded its range into the middle latitudes of the U.S., and one of the few mammals that invaded North America from South America. It is one of few placentals that withstand considerable decrease of body temperature without torpor. It presents a resting body temperature that is low and variable for a placental mammal of its size [9] and is the only vertebrate that gives birth to monozygotic quadruplets. Among 42 monotreme, marsupial and placental genera, Dasypus novemcinctus shows the highest variation of thoracolumbar vertebral count [10].
The particularities of Dasypus novemcinctus regarding vertebral count variation and ability to withstand variable temperature qualify it as a target organism for study of the relationship between skeleton morphology and temperature in mammals.
Knight et al. [8] explored variability in vertebral count within Dasypus novemcinctus to understand whether temperature during development determines skeleton morphology. To this end they experimented with 22 armadillos (19 with data) and litters from 12 pregnant females, in two environments, for three years — an impressive effort and experimental setup. Moreover, they used a wide variety of advanced experimental and analytical techniques. For example, they implanted intra-abdominal, long-term temperature recorders, which recorded data every 6 to 120 minutes for up to several months. They analysed body temperature periodicity by approximation of the recordings with Fourier series, and they CT-scanned fetuses.
All 19 individuals (from which data could be gathered) exhibited substantial daily variation in body temperature. Several intriguing results emerged such as the counter-intuitive finding that the mammals’ body temperature fluctuates more indoors than outdoors. Furthermore, three females (out of 12) were found to have offspring with atypical skeletons, and two of these mothers presented an extremely low internal temperature early in pregnancy. Additionally, genetically identical quadruplets differed skeletally among themselves within two litters.
Results are not yet definitive about the relationship of temperature during development and vertebral count in Dasypus novemcinctus. However, Knight et al. [8] demonstrated that nine-banded armadillos survive with high daily internal temperature fluctuations and successfully bring to term offspring which vary in skeletal morphology among and within genetically identical litters despite major temperature extremes.

References

[1] Hautier L, Weisbecker V, Sánchez-Villagra MR, Goswami A, Asher RJ (2010) Skeletal development in sloths and the evolution of mammalian vertebral patterning. Proceedings of the National Academy of Sciences, 107, 18903–18908. doi: 10.1073/pnas.1010335107
[2] Jordan, D.S. (1892) Relations of temperature to vertebrae among fishes. Proceedings of the United States National Museum, 1891, 107-120. doi: 10.5479/si.00963801.14-845.107
[3] Tibblin P, Berggren H, Nordahl O, Larsson P, Forsman A (2016) Causes and consequences of intra-specific variation in vertebral number. Scientific Reports, 6, 1–12. doi: 10.1038/srep26372
[4] Peabody RB, Brodie ED (1975) Effect of temperature, salinity and photoperiod on the number of trunk vertebrae in Ambystoma maculatum. Copeia, 1975, 741–746. doi: 10.2307/1443326
[5] Lindsey CC, Moodie GEE (1967) The effect of incubation temperature on vertebral count in the chicken. Canadian Journal of Zoology, 45, 891–892. doi: 10.1139/z67-099
[6] Galis F, Dooren TJMV, Feuth JD, Metz JAJ, Witkam A, Ruinard S, Steigenga MJ, Wunaendts LCD (2006) Extreme selection in humans against homeotic transformations of cervical vertebrae. Evolution, 60, 2643–2654. doi: 10.1111/j.0014-3820.2006.tb01896.x
[7] Buchholtz EA, Stepien CC (2009) Anatomical transformation in mammals: developmental origin of aberrant cervical anatomy in tree sloths. Evolution and Development, 11, 69–79. doi: 10.1111/j.1525-142X.2008.00303.x
[8] Knight F, Connor C, Venkataramanan R, Asher RJ. (2020). Body temperatures, life history, and skeletal morphology in the nine-banded armadillo (Dasypus novemcinctus). PCI-Ecology. doi: 10.17863/CAM.50971
[9] McNab BK (1980) Energetics and the limits to a temperate distribution in armadillos. Journal of Mammalogy, 61, 606–627. doi: 10.2307/1380307
[10] Asher RJ, Lin KH, Kardjilov N, Hautier L (2011) Variability and constraint in the mammalian vertebral column. Journal of Evolutionary Biology, 24, 1080–1090. doi: 10.1111/j.1420-9101.2011.02240.x

Tritrophic interactions have a central role in ecological theory and applications [1-3]. Particularly, systems comprised of plants, herbivores and predators have historically received wide attention given their ubiquity and economic importance [4]. Although ecologists have long aimed to understand the forces that govern alternating ecological effects at successive trophic levels [5], several key open questions remain (at least partially) unanswered [6]. In particular, the analysis of complex food webs has questioned whether ecosystems can be viewed as a series of trophic chains [7,8]. Moreover, whether systems are mostly controlled by top-down (trophic cascades) or bottom-up processes remains an open question [6].
Traditionally, studies have addressed how species diversity at different food chain compartments affect the strength and direction of trophic cascades [9]. For example, many studies have tested whether biological control was more efficient with more than one species of natural enemies [10-12]. Much less attention has been given to the role of within-species variation in shaping trophic cascades [13]. In particular, whereas the impact of trait variation within species of plants or predators on successive trophic levels has been recently addressed [14,15], the impact of intraspecific herbivore variation is in its infancy (but see [16]). This is at odds with the resurgent acknowledgment of the importance of individual variation for several ecological processes operating at higher levels of biological organization [17].
Sources of variation within species can come in many flavours. In herbivores, striking ecological variation can be found among populations occurring on different host plants, which become genetically differentiated, thus forming host races [18,19]. Curiously, the impact of variation across host races on the strength of trophic cascades has, to date, not been explored. This is the gap that the manuscript by Sentis and colleagues [20] fills. They experimentally studied a curious tri-trophic system where the primary consumer, pea aphids, specializes in different plant hosts, creating intraspecific variation across biotypes. Interestingly, there is also ecological variation across lineages from the same biotype. The authors set up experimental food chains, where pea aphids from different lineages and biotypes were placed in their universal legume host (broad bean plants) and then exposed to a voracious but charming predator, ladybugs. The full factorial design of this experiment allowed the authors to measure vertical effects of intraspecific variation in herbivores on both plant productivity (top-down) and predator individual growth (bottom-up).
The results nicely uncover the mechanisms by which intraspecific differences in herbivores precipitates vertical modulation in food chains. Herbivore lineage and host-plant specialization shaped the strength of trophic cascades, but curiously these effects were not modulated by density-dependence. Further, ladybugs consuming pea aphids from different lineages and biotypes grew at distinct rates, revealing bottom-up effects of intraspecific variation in herbivores.
These findings are novel and exciting for several reasons. First, they show how intraspecific variation in intermediate food chain compartments can simultaneously reverberate both top-down and bottom-up effects. Second, they bring an evolutionary facet to the understanding of trophic cascades, providing valuable insights on how genetically differentiated populations play particular ecological roles in food webs. Finally, Sentis and colleagues’ findings [20] have critical implications well beyond their study systems. From an applied perspective, they provide an evident instance on how consumers’ evolutionary specialization matters for their role in ecosystems processes (e.g. plant biomass production, predator conversion rate), which has key consequences for biological control initiatives and invasive species management. From a conceptual standpoint, their results ignite the still neglected value of intraspecific variation (driven by evolution) in modulating the functioning of food webs, which is a promising avenue for future theoretical and empirical studies.

References

[1] Price, P. W., Bouton, C. E., Gross, P., McPheron, B. A., Thompson, J. N., & Weis, A. E. (1980). Interactions among three trophic levels: influence of plants on interactions between insect herbivores and natural enemies. Annual review of Ecology and Systematics, 11(1), 41-65. doi: 10.1146/annurev.es.11.110180.000353
[2] Olff, H., Brown, V.K. & Drent, R.H. (1999). Herbivores: between plants and predators. Blackwell Science, Oxford.
[3] Tscharntke, T. & Hawkins, B.A. (2002). Multitrophic level interactions. Cambridge University Press. doi: 10.1017/CBO9780511542190
[4] Agrawal, A. A. (2000). Mechanisms, ecological consequences and agricultural implications of tri-trophic interactions. Current opinion in plant biology, 3(4), 329-335. doi: 10.1016/S1369-5266(00)00089-3
[5] Pace, M. L., Cole, J. J., Carpenter, S. R., & Kitchell, J. F. (1999). Trophic cascades revealed in diverse ecosystems. Trends in ecology & evolution, 14(12), 483-488. doi: 10.1016/S0169-5347(99)01723-1
[6] Abdala‐Roberts, L., Puentes, A., Finke, D. L., Marquis, R. J., Montserrat, M., Poelman, E. H., ... & Mooney, K. (2019). Tri‐trophic interactions: bridging species, communities and ecosystems. Ecology letters, 22(12), 2151-2167. doi: 10.1111/ele.13392
[7] Polis, G.A. & Winemiller, K.O. (1996). Food webs. Integration of patterns and dynamics. Chapmann & Hall, New York. doi: 10.1007/978-1-4615-7007-3
[8] Torres‐Campos, I., Magalhães, S., Moya‐Laraño, J., & Montserrat, M. (2020). The return of the trophic chain: Fundamental vs. realized interactions in a simple arthropod food web. Functional Ecology, 34(2), 521-533. doi: 10.1111/1365-2435.13470
[9] Polis, G. A., Sears, A. L., Huxel, G. R., Strong, D. R., & Maron, J. (2000). When is a trophic cascade a trophic cascade?. Trends in Ecology & Evolution, 15(11), 473-475. doi: 10.1016/S0169-5347(00)01971-6
[10] Sih, A., Englund, G., & Wooster, D. (1998). Emergent impacts of multiple predators on prey. Trends in ecology & evolution, 13(9), 350-355. doi: 10.1016/S0169-5347(98)01437-2
[11] Diehl, E., Sereda, E., Wolters, V., & Birkhofer, K. (2013). Effects of predator specialization, host plant and climate on biological control of aphids by natural enemies: a meta‐analysis. Journal of Applied Ecology, 50(1), 262-270. doi: 10.1111/1365-2664.12032
[12] Snyder, W. E. (2019). Give predators a complement: conserving natural enemy biodiversity to improve biocontrol. Biological control, 135, 73-82. doi: 10.1016/j.biocontrol.2019.04.017
[13] Des Roches, S., Post, D. M., Turley, N. E., Bailey, J. K., Hendry, A. P., Kinnison, M. T., ... & Palkovacs, E. P. (2018). The ecological importance of intraspecific variation. Nature Ecology & Evolution, 2(1), 57-64. doi: 10.1038/s41559-017-0402-5
[14] Bustos‐Segura, C., Poelman, E. H., Reichelt, M., Gershenzon, J., & Gols, R. (2017). Intraspecific chemical diversity among neighbouring plants correlates positively with plant size and herbivore load but negatively with herbivore damage. Ecology Letters, 20(1), 87-97. doi: 10.1111/ele.12713
[15] Start, D., & Gilbert, B. (2017). Predator personality structures prey communities and trophic cascades. Ecology letters, 20(3), 366-374. doi: 10.1111/ele.12735
[16] Turcotte, M. M., Reznick, D. N., & Daniel Hare, J. (2013). Experimental test of an eco-evolutionary dynamic feedback loop between evolution and population density in the green peach aphid. The American Naturalist, 181(S1), S46-S57. doi: 10.1086/668078
[17] Bolnick, D. I., Amarasekare, P., Araújo, M. S., Bürger, R., Levine, J. M., Novak, M., ... & Vasseur, D. A. (2011). Why intraspecific trait variation matters in community ecology. Trends in ecology & evolution, 26(4), 183-192. doi: 10.1016/j.tree.2011.01.009
[18] Drès, M., & Mallet, J. (2002). Host races in plant–feeding insects and their importance in sympatric speciation. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, 357(1420), 471-492. doi: 10.1098/rstb.2002.1059
[19] Magalhães, S., Forbes, M. R., Skoracka, A., Osakabe, M., Chevillon, C., & McCoy, K. D. (2007). Host race formation in the Acari. Experimental and Applied Acarology, 42(4), 225-238. doi: 10.1007/s10493-007-9091-0
[20] Sentis, A., Bertram, R., Dardenne, N., Simon, J.-C., Magro, A., Pujol, B., Danchin, E. and J.-L. Hemptinne (2020) Intraspecific difference among herbivore lineages and their host-plant specialization drive the strength of trophic cascades. bioRxiv, 722140, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/722140

The concept of holobiont dates back to more than thirty years, it was primarily coined to hypothesize the importance of symbiotic associations to generate significant evolutionary novelties. Quickly adopted to describe the now well-studied system formed by zooxanthella associated corals, this concept expanded much further after the emergence of High-Throughput Sequencing and associated progresses in metabarcoding and metagenomics.
Holobionts – defined as the association between an individual host and its microbiota - are now increasingly described at sea and on land. The opinion article by Dittami et al. [1] provides a synthetic overview of marine holobionts. It retraces the history of the holobiont concept, recalls the main mechanisms underlying the association between hosts and microbial communities, highlights the influence of these symbioses on marine ecosystem functioning, and outlines current tools and future lines of research.
In particular, the article discusses some particularities of marine systems, such as the strong connectivity allowing an exchange of microorganisms and chemical signals between and within holobionts.
The authors advocate the need to bridge the gap between large scale exploration studies and smaller scale mechanistic studies, by conducting interdisciplinary research (combining physiology, biochemistry, ecology, experimentation and computational modeling) on some keystone holobionts.
Finally, one strength of the paper by Dittami et al. [1] is that it places the concept of the holobiont in an applied research framework. Several possible applications of knowledge on host-microbiota interactions are suggested, both in the field of aquaculture and that of monitoring the health of marine ecosystems. This article contains all the necessary elements for someone who would like to jump into the study of the holobionths in the marine world.

References
[1] Dittami SM, Arboleda E, Auguet J, Bigalke A, Briand E, Cardenas P, Cardini U, Decelle J, Engelen AH, Eveillard D, Gachon CMM, Griffiths SM, Harder T, Kayal E, Kazamia E, Lallier FH, Medina M, Marzinelli E, Morganti T, Núñez Pons L, Prado S, Pintado J, Saha M, Selosse M, Skillings D, Stock W, Sunagawa S, Toulza E, Vorobev A, Leblanc C, Not F. (2020). A community perspective on the concept of marine holobionts: current status, challenges, and future directions. Zenodo, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.5281/zenodo.3696771

Functional traits are “morpho-physio-phenological traits which impact fitness indirectly via their effects on growth, reproduction and survival” [1]. Most functional traits are defined at organ level, e.g. for leaves, roots and stems, and reflect key aspects of resource acquisition and resource use by organisms for their development and reproduction [2]. More rarely, some functional traits can be related to spatial development, such as vegetative height and lateral spread in plants.
Organ-level traits are especially popular because they can be measured in a standard way and easily compared over many plants. But these traits can broadly vary during the life of an organism. For instance, Roggy et al. [3] found that Leaf Mass Area can vary from 30 to 140 g.m^(-2) between seedling and adult stages for the canopy tree Dicorynia guianensis in French Guiana. Fortunel et al. [4] have also showed that developmental stages much contribute to functional trait variation within several Micropholis tree species in lowland Amazonia.
The way plants grow and invest resources into organs is variable during life and allows defining specific developmental sequences and architectural models [5,6]. There is clear ontogenic variation in leaf number, leaf properties and ramification patterns. Ontogenic variations reflect changing adaptation of an individual over its life, depending on the changing environmental conditions.
In this regard, measuring a single functional trait at organ level in adult trees should miss the variation of resource acquisition and use strategies over time. Thus we should built a more integrative approach of ecological development, also called “eco-devo” approach [7].
Although the ecological significance of ontogeny and developmental strategies is now well known, the extent to which it contributes to explain species survival and coexistence in communities is still broadly ignored in functional ecology. Levionnois et al. [8] investigated intraspecific variation of functional traits and growth trajectories in a typical, early-successional tree species in French Guiana, Amazonia. This species, Cecropia obtusa, is generalist regarding soil type and can be found on both white sand and ferralitic soil. The study examines whether there in intraspecific variation in functional traits and growth trajectories of C. obtusa in response to the contrasted soil types.
The tree communities observed on the two types of soils include species with distinctive functional trait values, that is, there are changes in species composition related to different species strategies along the classical wood and leaf economic spectra. The populations of C. obtusa found on the two soils showed some difference in functional traits, but it did not concern traits related to the main economic spectra. Conversely, the populations showed different growth strategies, in terms of spatial and temporal development.
The major lessons we can learn from the study are:
(i) Functional traits measured at organ level cannot reflect well how long-lived plants collect and invest resources during their life. The results show the potential of considering architectural and developmental traits together with organ-level functional traits, to better acknowledge the variation in ecological strategies over plant life, and thus to better understand community assembly processes.
(ii) What makes functional changes between communities differs when considering interspecific and intraspecific variation. Species turnover should encompass different corteges of soil specialists. These specialists are sorted along economic spectra, as shown in tropical rainforests and globally [2]. Conversely, a generalist species such as C. obtusa does occur on contrasted soil, which entails that it can accommodate the contrasted ecological conditions. However, the phenotypic adjustment is not related to how leaves and wood ensure photosynthesis, water and nutrient acquisition, but regards the way the resources are allocated to growth and reproduction over time.
The results of the study stress the need to better integrate growth strategies and ontogeny in the research agenda of functional ecology. We can anticipate that organ-level functional traits and growth trajectories will be more often considered together in ecological studies. The integration should help better understand the temporal niche of organisms, and how organisms can coexist in space and time with other organisms during their life. Recently, Klimešová et al. [9] have proposed standardized protocols for collecting plant modularity traits. Such effort to propose easy-to-measure traits representing plant development and ontogeny, with clear functional roles, should foster the awaited development of an “eco-devo” approach.

References

[1] Violle, C., Navas, M. L., Vile, D., Kazakou, E., Fortunel, C., Hummel, I., & Garnier, E. (2007). Let the concept of trait be functional!. Oikos, 116(5), 882-892. doi: 10.1111/j.0030-1299.2007.15559.x
[2] Díaz, S. et al. (2016). The global spectrum of plant form and function. Nature, 529(7585), 167-171. doi: 10.1038/nature16489
[3] Roggy, J. C., Nicolini, E., Imbert, P., Caraglio, Y., Bosc, A., & Heuret, P. (2005). Links between tree structure and functional leaf traits in the tropical forest tree Dicorynia guianensis Amshoff (Caesalpiniaceae). Annals of forest science, 62(6), 553-564. doi: 10.1051/forest:2005048
[4] Fortunel, C., Stahl, C., Heuret, P., Nicolini, E. & Baraloto, C. (2020). Disentangling the effects of environment and ontogeny on tree functional dimensions for congeneric species in tropical forests. New Phytologist. doi: 10.1111/nph.16393
[5] Barthélémy, D., & Caraglio, Y. (2007). Plant architecture: a dynamic, multilevel and comprehensive approach to plant form, structure and ontogeny. Annals of botany, 99(3), 375-407. doi: 10.1093/aob/mcl260
[6] Hallé, F., & Oldeman, R. A. (1975). An essay on the architecture and dynamics of growth of tropical trees. Kuala Lumpur: Penerbit Universiti Malaya.
[7] Sultan, S. E. (2007). Development in context: the timely emergence of eco-devo. Trends in Ecology & Evolution, 22(11), 575-582. doi: 10.1016/j.tree.2007.06.014
[8] Levionnois, S., Tysklind, N., Nicolini, E., Ferry, B., Troispoux, V., Le Moguedec, G., Morel, H., Stahl, C., Coste, S., Caron, H. & Heuret, P. (2020). Soil variation response is mediated by growth trajectories rather than functional traits in a widespread pioneer Neotropical tree. bioRxiv, 351197, ver. 4 peer-reviewed and recommended by PCI Ecology. doi: 10.1101/351197
[9] Klimešová, J. et al. (2019). Handbook of standardized protocols for collecting plant modularity traits. Perspectives in Plant Ecology, Evolution and Systematics, 40, 125485. doi: 10.1016/j.ppees.2019.125485