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Chemosensory speciation (chemosensory isolation) is the evolution of a population to become distinct species that is driven by chemical stimuli (i.e., chemical signals, recognition). These chemical signals may create premating or other isolating behavioral barriers that prevent gene flow among subpopulations that eventually lead to two separate species.[1]

Chemosensory pathways are vital for exogenous and endogenous recognition and processing of volatile organic compounds (VOCs);[2] therefore, they are viewed as active attributors to an organism's behavior.[1][3] Chemosensory pathways involving: odorant binding proteins (OBP), chemosensory proteins (CSP), gustatory receptors (GR), and sensory neuron membrane proteins (SNMP), have been investigated in numerous biological systems as genetic barriers. These chemosensory genes are utilized for identification of candidate loci that are under positive selection. Experiments are commonly tailored to studying an organism's response to alterations in their chemosensory pathways, or using molecular phylogenetics to analyze the divergence of these systems in sister taxa. Sensory pathways allow integration of environmental stimuli that strongly influence an organism's behavior and are hypothesized to have broad implications as a module of behavioral selection;[2] nevertheless, here it will be reviewed briefly in three well-supported modules: Resource Identification (foraging behaviors), Conspecific Interactions (sexual selection), and Host Recognition.

Resource identification

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In vivo, a complex of chemical signals and pheromones are commonly perceived together instead of as chemical isolates. Identification of specific chemical cues in the myriad of surrounding compounds commonly leads to behavioral changes in the recipient organism. For instance, in a recent publication studying behavioral phenotypes, the researchers identify a foraging behavioral shift that is caused by an insensitivity to one of several pheromone isoforms detected in the mutant and wildtype; the pheromone insensitivity stimulates a constant foraging behavior, despite regular activity performed by the other individuals in the population.[4] The expansion and evolution of chemosensory systems are especially evident in the insect lineage due to their life history. For example, a recent publication highlights the importance of odorant receptors (OR) for proper antennal lobe (AL) function; a gene knockout of an OR co-receptor drastically impaired AL development in the clonal raider ant, Ooceraea biroi.[5] Chemosensory systems, and their regulatory repertoire, influence the development and behavior of foraging organisms.[6]

Host recognition

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Regardless of the relationship (symbiont, commensal, or parasitic), host recognition is determined by deciphering the surrounding chemical cocktails for specific signals that excite their sensory receptors. Host race formation in Aphid species has recently been used as a model system to understand divergent selection in the face of gene flow.[7][8] For populations that depend on a host, their ability to identify and locate host signals are recognized as being under a post-mating selection pressure. The host-dependent organisms harbor sensory adaptations that allow them to appropriately process complex mixtures of chemical cues.[9] Intermating populations that are host specific may have a higher chance of allopatric isolation and divergence due to a narrowed niche and host’s ecological variability.[10] Another evolutionary model that supports chemosensory importance is the antagonistic Red Queen hypothesis that elaborates on coevolution adaptations.[11]

Conspecific interaction

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Olfactory cues are widely used for conspecific and mate selection but are also commonly used in avoidance strategies. The role of chemosensory systems in conspecific recognition recapitulates their place in natural and sexual selection. Chemosensory cues offer initial information on potential mates, such as size, age, and environment.[12] An organism’s integration of these cues allows them to choose mates that provide increased fitness. Divergence of pheromones and their receptors lead to various expression patterns within populations that may then be selected upon. This variation of hormone expression has been studied in numerous biological systems.[13] For example, two populations that are not spatially isolated, yet form a species complex with several monophyletic types may require specific chemical identification for proper intraspecific communication and mate selection.[14] An example of this intraspecific communication barrier is seen in two co-habitual populations of the Iberian wall lizard, Podarcis hispanica; the males of the two species emit different pheromone assemblages and can discriminate the types of cues, however, the females were unable to discriminate between the two pheromone cues.[14] The behavioral and evolutionary impacts of these relationships are commonly underlined in more recent sexual selection models, such as the good genes (sexy son hypothesis) and the sensory bias model.[15][16][17]

References

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  1. ^ a b Smadja C, Butlin RK (January 2009). "On the scent of speciation: the chemosensory system and its role in premating isolation". Heredity. 102 (1): 77–97. doi:10.1038/hdy.2008.55. PMID 18685572. S2CID 25964561.
  2. ^ a b Vieira FG, Rozas J (2011-01-01). "Comparative genomics of the odorant-binding and chemosensory protein gene families across the Arthropoda: origin and evolutionary history of the chemosensory system". Genome Biology and Evolution. 3: 476–90. doi:10.1093/gbe/evr033. PMC 3134979. PMID 21527792.
  3. ^ Smadja C, Ganem G (2008-01-01). "Divergence of odorant signals within and between the two European subspecies of the house mouse". Behavioral Ecology. 19 (1): 223–230. doi:10.1093/beheco/arm127. ISSN 1045-2249.
  4. ^ Greene JS, Brown M, Dobosiewicz M, Ishida IG, Macosko EZ, Zhang X, et al. (November 2016). "Balancing selection shapes density-dependent foraging behaviour". Nature. 539 (7628): 254–258. Bibcode:2016Natur.539..254G. doi:10.1038/nature19848. PMC 5161598. PMID 27799655.
  5. ^ Ryba AR, McKenzie SK, Olivos-Cisneros L, Clowney EJ, Pires PM, Kronauer DJ (August 2020). "Comparative Development of the Ant Chemosensory System". Current Biology. 30 (16): 3223–3230.e4. doi:10.1016/j.cub.2020.05.072. PMC 7438299. PMID 32559450.
  6. ^ van Schooten B, Meléndez-Rosa J, Van Belleghem SM, Jiggins CD, Tan JD, McMillan WO, Papa R (July 2020). "Divergence of chemosensing during the early stages of speciation". Proceedings of the National Academy of Sciences of the United States of America. 117 (28): 16438–16447. Bibcode:2020PNAS..11716438V. doi:10.1073/pnas.1921318117. PMC 7371972. PMID 32601213.
  7. ^ Eyres I, Duvaux L, Gharbi K, Tucker R, Hopkins D, Simon JC, et al. (January 2017). "Targeted re-sequencing confirms the importance of chemosensory genes in aphid host race differentiation". Molecular Ecology. 26 (1): 43–58. Bibcode:2017MolEc..26...43E. doi:10.1111/mec.13818. PMC 6849616. PMID 27552184.
  8. ^ Diehl SR, Bush GL (1984-01-01). "An Evolutionary and Applied Perspective of Insect Biotypes". Annual Review of Entomology. 29 (1): 471–504. doi:10.1146/annurev.en.29.010184.002351. ISSN 0066-4170.
  9. ^ Kulmuni J, Wurm Y, Pamilo P (June 2013). "Comparative genomics of chemosensory protein genes reveals rapid evolution and positive selection in ant-specific duplicates". Heredity. 110 (6): 538–47. doi:10.1038/hdy.2012.122. PMC 3656642. PMID 23403962.
  10. ^ Drès M, Mallet J (April 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): 471–92. doi:10.1098/rstb.2002.1059. PMC 1692958. PMID 12028786.
  11. ^ Morran LT, Schmidt OG, Gelarden IA, Parrish RC, Lively CM (July 2011). "Running with the Red Queen: host-parasite coevolution selects for biparental sex". Science. 333 (6039): 216–8. Bibcode:2011Sci...333..216M. doi:10.1126/science.1206360. PMC 3402160. PMID 21737739.
  12. ^ Shine R, Phillips B, Waye H, LeMaster M, Mason RT (2003-07-01). "Chemosensory cues allow courting male garter snakes to assess body length and body condition of potential mates". Behavioral Ecology and Sociobiology. 54 (2): 162–166. doi:10.1007/s00265-003-0620-5. ISSN 1432-0762. S2CID 22852516.
  13. ^ Deisig N, Kropf J, Vitecek S, Pevergne D, Rouyar A, Sandoz JC, et al. (2012-03-12). "Differential interactions of sex pheromone and plant odour in the olfactory pathway of a male moth". PLOS ONE. 7 (3): e33159. Bibcode:2012PLoSO...733159D. doi:10.1371/journal.pone.0033159. PMC 3299628. PMID 22427979.
  14. ^ a b Martín J, López P (2006-03-01). "Interpopulational differences in chemical composition and chemosensory recognition of femoral gland secretions of male lizards Podarcis hispanica: implications for sexual isolation in a species complex". Chemoecology. 16 (1): 31–38. Bibcode:2006Checo..16...31M. doi:10.1007/s00049-005-0326-4. ISSN 1423-0445. S2CID 32881016.
  15. ^ Fuller RC, Houle D, Travis J (October 2005). "Sensory bias as an explanation for the evolution of mate preferences". The American Naturalist. 166 (4): 437–46. doi:10.1086/444443. PMID 16224700. S2CID 4849390.
  16. ^ Egger B, Klaefiger Y, Theis A, Salzburger W (2011-10-18). "A sensory bias has triggered the evolution of egg-spots in cichlid fishes". PLOS ONE. 6 (10): e25601. Bibcode:2011PLoSO...625601E. doi:10.1371/journal.pone.0025601. PMC 3196499. PMID 22028784.
  17. ^ Weatherhead PJ, Robertson RJ (1979-02-01). "Offspring Quality and the Polygyny Threshold: "The Sexy Son Hypothesis"". The American Naturalist. 113 (2): 201–208. doi:10.1086/283379. ISSN 0003-0147. S2CID 85283084.
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