Evolutionary Ecology of Specialisation

Abstract

The processes that drive the evolution of specialisation are still poorly understood. While theory generally invokes the assumption that generalists bear costs compared to species that have a less intense exploitation of specific resources, the existence of these costs have not received strong empirical support. Recent studies have broadened the dialogue by examining specialisation from a macroevolutionary perspective. Are specialist lineages transitioning towards a broader niche under certain environmental conditions, or are they limited in their evolutionary potential and doomed to eventual extinction? The overall finding is that context dependency is key to driving rapid transitions in niche dimensions and composition. Answers to these questions are fascinating in terms of better understanding the natural world and also have the potential to improve prioritisation of future conservation efforts.

Key Concepts

  • Many ideas about the evolution of specialisation rely on the premise that ‘Jack of all trades is master of none’, that is, generalists are locally outperformed by specialists.
  • Genetic or physiological trade‐offs imply that populations experience reduced performance in one function when selection results in increased performance on another function (antagonistic pleiotropy).
  • The evolution of specialisation depends on how often alternate hosts or environments are encountered, which depends on abundance and range extent of a species and its neighbours.
  • Biogeography, functional trait distributions and range limits create ‘forbidden links’ by precluding pairs of species, or a species and a particular suite of environmental variables, from coexisting.
  • The idea of specialisation applies equally to a species biotic and abiotic niche, yet the expectations for how specialisation may evolve for each aspect of niche may differ.
  • Evolutionary transitions from specialisation to generalisation are common (and vice versa), yet specialists may experience greater extinction rates due to smaller geographical range.
  • The evolutionary ecology of specialisation is emerging as a key component in studies of host–pathogen evolution and conservation biology.

Keywords: interactions; population ecology; ecological networks; community ecology; species interactions; community ecology

Figure 1. Fitness trade‐offs for fungi on A. strigosus versus L. bicolour. Bradyrhizobium cultured from L. bicolour performed better on L. bicolour and vice versa of Bradyrhizobium cultured from A. strigosus. Success of Bradyrhizobium genotypes isolated from conspecific versus allospecific hosts. Closed circles indicate growth of A. strigosus test plants; open circles indicate growth of L. bicolor test plants. Error bars represent ±1 standard error. (Reproduced from Ehlinger et al. (2014) © BioMed Central).
Figure 2. The effects of environmental variance on the evolution of specialisation. Solid bold arrows reflect positive relationships and fine dashed arrows reflect negative relationships (the effects of productivity and complexity of the environment are relatively unknown). All of these factors contribute to manifestation of specialised interactions between organisms (e.g. plant–pollinator interactions whereby both partners harbour a suite of matching traits). The image here depicts a sunbird getting its food from the bottom of an aloe flower, while receiving pollen on its head. It will deliver this pollen to the next visited plant, thus achieving pollination for the aloe plant. The shape of its beak and head allows it to match the flower morphology. The extent to which habitat specialisation of aloes (Aloe sp. are largely restricted to arid environments) increases the predictability of interactions with certain pollinators and fosters the evolution of biotic specialisation requires further study. (Reproduced from Poisot et al. (2011) © The National Center for Biotechnology Information.)
Figure 3. Phylogenetic (a) and geographical (b) specificity patterns. (Reproduced with permission from Barrett LG and Heil M. (2012) © Elsevier).
Figure 4. (a) The versatility of pollinators is often a function of their mouthparts (figure modified from Fontaine et al., ) that either allow or prevent access to the rewards, especially to restrictive flowers. The restrictiveness of flowers is often a trait that exhibits phylogenetic signal in communities (e.g. closely related species will exhibit similarity in floral restrictiveness) and this will translate into certain pollinators exhibiting a higher degree of phylogenetic specificity (b). In (b), plants that have restrictive flowers (e.g. tubular, dark blue circles on the left) restrict visits from pollinators with short tongues (e.g. syrphids; light blue circles on the right). Long‐tongued pollinators (dark blue circles on the right) have fewer forbidden links than short‐tongued pollinators and, thus, unrestrictive flowers (light blue circles on the left may receive visits from a more diverse set of pollinators. (Reproduced from Vamosi JC, Moray CM, Garcha NK, Chamberlain SA, and Mooers AØ. (2014) © John Wiley and Sons Ltd. Published under the terms of the Creative Commons Attribution License.)
close

References

Alarcón R, Waser NM and Ollerton J (2008) Year‐to‐year variation in the topology of a plant–pollinator interaction network. Oikos 117: 1796–1807.

Armbruster WS and Baldwin BG (1998) Switch from specialized to generalized pollination. Nature 394: 621.

Armbruster WS (2014) Floral specialization and angiosperm diversity: phenotypic divergence, fitness trade‐offs and realized pollination accuracy. Annals of Botany 6: plu003.

Barrett LG and Heil M (2012) Unifying concepts and mechanisms in the specificity of plant–enemy interactions. Trends in Plant Science 17: 1360–1385.

Bonetti MF and Wiens JJ (2014) Evolution of climatic niche specialization: a phylogenetic analysis in amphibians. Proceedings of the Royal Society of London B 281: 20133229. DOI: http://dx.doi.org/10.1098/rspb.2013.3229.

Bridle J, Gavaz S and Kennington WJ (2009) Testing limits to adaptation along altitudinal gradients in rainforest Drosophila. Proceedings of the Royal Society of London B 276: 1507–1515.

Bridle JR, Buckley J, Bodsorth EJ and Thomas CD (2013) Evolution on the move: specialization on widespread resources associated with rapid range expansion in response to climate change. Proceedings of the Royal Society of London B 281: 20131800.

Brown JS and Pavlovic NB (1992) Evolution in heterogeneous environments: effects of migration on habitat specialization. Evolutionary Ecology 6: 360–382.

Buckley LB, Davies TJ, Ackerly DD, et al. (2010) Phylogeny, niche conservatism and the latitudinal diversity gradient in mammals. Proceedings of the Royal Society B: Biological Sciences 277 (1691): 2131–2138.

Colles A, Liow LH and Prinzing A (2009) Are specialists at risk under environmental change? Neoecological, paleoecological and phylogenetic approaches. Ecology Letters 12: 849–863.

Cooper VS and Lenski RE (2000) The population genetics of ecological specialization in evolving Escherichia coli populations. Nature 407: 736–739.

Davies TJ and Pedersen AB (2008) Phylogeny and geography predict pathogen community similarity in wild primates and humans. Proceedings of the Royal Society of London B 275: 1695–1701.

Débarre F and Gandon S (2010) Evolution of specialization in a spatially continuous environment. Journal of Evolutionary Biology 23: 1090–1099.

Devictor V, Clavel J, Julliard R, et al. (2010) Defining and measuring ecological specialization. Journal of Applied Ecology 47: 15–25.

Edwards EJ, Osborne CP, Strömberg CAE, Smith SA and Consortium CG (2010) The origins of C4 grasslands: integrating evolutionary and ecosystem science. Science 328: 587–591.

Ehlinger M, Mohr T, Starcevich J, et al. (2014) Specialization‐generalization trade‐off in a Bradyrhizobium symbiosis with wild legume hosts. BMC Ecology 14: 8.

Engering A, Hogerwerf L and Slingernbergh J (2013) Pathogen–host–environment interplay and disease emergence. Emerging Microbes & Infections 2: e5.

Fenster CB, Armbruster WS, Wilson P, Thomson JD and Dudash MR (2004) Pollination syndromes and floral specialization. Annual Review of Ecology, Evolution, and Systematics 35: 375–403.

Fontaine C, Dajoz I, Meriguet J and Loreau M (2006) Functional diversity of plant–pollinator interaction webs enhances the persistence of plant communities. PLoS Biology 4 (1): e1. DOI: 10.1371/journal.pbio.0040001.

Futuyma DJ and Moreno G (1988) The evolution of ecological specialization. Annual Review of Ecological Systems 19: 207–233.

Joshi A and Thompson JN (1995) Trade‐offs and the evolution of host specialization. Evolutionary Ecology 9: 82–92.

Kassen R (2002) The experimental evolution of specialists, generalists, and the maintenance of diversity. Journal of Evolutionary Biology 15: 173–190.

Kawecki TJ (1994) Accumulation of deleterious mutations and the evolutionary cost of being a generalist. American Naturalist 144: 833–838.

Kay KM and Sargent RD (2009) The role of animal pollination in plant speciation: integrating ecology, geography and genetics. Annual Review of Ecology, Evolution, and Systematics 40: 637–656.

Kelley ST and Farrell BD (1998) Is specialization a dead end? The phylogeny of host use in dendroctonus bark beetles (Scolytidae). Evolution 52: 1731–1743.

Kirkpatrick M and Barton NH (1997) Evolution of a species' range. American Naturalist 150: 1–23.

Muschick M, Nosil P, Harmon LJ and Salzburger W (2014) Ecological niche dimensionality and the stages of adaptive radiation of cichlids within Lake Tanganyika Proc. Royal Society of London. Series B 281.

Nosil P (2002) Transition rates between specialization and generalization in phytophagous insects. Evolution 56: 1701–1706.

Nosil P and Mooers AO (2005) Testing hypotheses about ecological specialization using phylogenetic trees. Evolution 59: 2256–2263.

Nuismer SL, Jordano P and Bascompte J (2013) Coevolution and the architecture of mutualistic networks. Evolution 67: 338–354.

Olesen JM, Bascompte J, Elberling H and Jordano P (2008) Temporal dynamics in a pollination network. Ecology 89: 1573–1582.

Parker IM, Saunders M, Bontrager M, et al. (2015) Phylogenetic structure and host abundance drive disease pressure in communities. Nature 520: 542–544.

Poisot T, Bever JD, Nemri A, Thrall PH and Hochberg ME (2011) A conceptual framework for the evolution of ecological specialisation. Ecology Letters 14: 841–851.

Poisot T, Stanko M, Miklisova D and Morand S (2013) Facultative and obligate parasite communities exhibit different network properties. Parasitology 140: 1340–1345.

Price TD and Kirkpatrick M (2009) Evolutionarily stable range limits set by interspecific competition. Proceedings of the Royal Society of London B 276: 1429–1434.

Rezende EL, Lavabre JE, Guimaraes PR, Jordano P and Bascompte J (2007) Non‐random coextinctions in phylogenetically structured mutualistic networks. Nature 448: 925–928.

Sargent RD and Vamosi JC (2008) The influence of canopy position, pollinator syndrome, and region on evolutionary transitions in pollinator guild size. International Journal of Plant Sciences 169: 39–47.

Stanley SM (1987) Extinction. New York: Scientific American Books.

Thomas CD, Bodsorth EJ, Wilson RJ, et al. (2001) Ecological and evolutionary processes at expanding range margins. Nature 411: 577–580.

Vamosi JC, Moray CM, Garcha NK, Chamberlain SA and Mooers AØ (2014) Pollinators visit related plant species across 29 plant–pollinator networks. Ecology and Evolution 4: 2303–2315.

Whitlock MC (1996) The Red Queen beats the Jack‐of‐all‐trades: the limitations on the evolution of phenotypic plasticity and niche breadth. American Naturalist 148: S65–S77.

Wiegmann B, Mitter C and Farrell B (1993) Diversification of carnivorous parasitic insects: extraordinary radiation or specialized dead end? American Naturalist 142: 737–754.

Williams SE, Williams YM, VanDerWal J, et al. (2009) Ecological specialization and population size in a biodiversity hotspot: how rare species avoid extinction. Proceedings of the National Academy of Sciences of the United States of America 17: 19737–19741.

Further Reading

Bolnick DI, Svanbäck R and Fordyce JA (2003) The ecology of individuals: incidence and implications of individual specialization. American Naturalist 161 (1): 1–28.

Morand S, Littlewod T and Poulin R (eds) (2015) Evolutionary Ecology of Host‐Parasite Systems. Cambridge: Cambridge University Press.

Poisot T, Thrall PH and Hochberg ME (2012) Trophic network structure emerges through antagonistic coevolution in temporally varying environments. Proceedings of the Royal Society B: Biological Sciences 279 (1712): 299–308.

Schluter D (2000) The Ecology of Adaptive Radiation. Oxford: Oxford University Press.

Wiens JJ, Ackerly DD, Allen AP, et al. (2010) Niche conservatism as an emerging principle in ecology and conservation biology. Ecology Letters 12 (10): 1310–1324.

Contact Editor close
Submit a note to the editor about this article by filling in the form below.

* Required Field

How to Cite close
Vamosi, Jana C, and Poisot, Timothée(Feb 2016) Evolutionary Ecology of Specialisation. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0026281]