Editing Coevolution (section)

=== Flowering plants ===

Flowers appeared and diversified relatively suddenly in the fossil record, creating what [[Charles Darwin]] described as the "abominable mystery" of how they had evolved so quickly; he considered whether coevolution could be the explanation.<ref name="CardinalDanforth2013"/><ref>{{cite journal |last=Friedman |first=W. E. |date=January 2009 |title=The meaning of Darwin's 'abominable mystery' |journal=American Journal of Botany |volume=96 |issue=1 |pages=5–21 |doi=10.3732/ajb.0800150 |pmid=21628174 }}</ref> He first mentioned coevolution as a possibility in ''[[On the Origin of Species]]'', and developed the concept further in ''[[Fertilisation of Orchids]]'' (1862).<ref name=t24>{{cite book |first=John N. |last=Thompson |title=The coevolutionary process |publisher=[[University of Chicago Press]] |location=Chicago |year=1994 |isbn=978-0-226-79760-1 |url=https://books.google.com/books?id=AyXPQzEwqPIC&q=Wallace+%22creation+by+law%22+Angr%C3%A6cum&pg=PA27 |access-date=2009-07-27}}</ref><ref name=origins94>{{cite book |last=Darwin |first=Charles |year=1859 |title=On the Origin of Species |edition=1st |location=London |publisher=John Murray |url=http://darwin-online.org.uk/content/frameset?itemID=F373&viewtype=text&pageseq=1 |access-date=2009-02-07}}</ref><ref name=orchids1>{{cite book |last=Darwin |first=Charles |year=1877 |title=On the various contrivances by which British and foreign orchids are fertilised by insects, and on the good effects of intercrossing |location=London |publisher=John Murray |edition=2nd |url=http://darwin-online.org.uk/content/frameset?itemID=F801&viewtype=text&pageseq=1 |access-date=2009-07-27}}</ref>

====Insects and insect-pollinated flowers====
{{Further|Entomophily}}
[[File:Apis mellifera - Melilotus albus - Keila.jpg|thumb|upright|[[Honey bee]] taking a reward of [[nectar]] and collecting pollen in its [[pollen basket]]s from [[Melilotus albus|white melilot]] flowers]]

Modern [[entomophily|insect-pollinated (entomophilous) flowers]] are conspicuously coadapted with insects to ensure pollination and in return to reward the [[pollinator]]s with nectar and pollen. The two groups have coevolved for over 100 million years, creating a complex network of interactions. Either they evolved together, or at some later stages they came together, likely with pre-adaptations, and became mutually adapted.<ref name=Lunau>{{cite journal |last=Lunau |first=Klaus |title=Adaptive radiation and coevolution — pollination biology case studies |journal=Organisms Diversity & Evolution |date=2004 |volume=4 |issue=3 |pages=207–224 |doi=10.1016/j.ode.2004.02.002 |doi-access= |bibcode=2004ODivE...4..207L }}</ref><ref>{{cite book |last=Pollan |first=Michael |author-link=Michael Pollan |title=The Botany of Desire: A Plant's-eye View of the World |publisher=Bloomsbury |isbn=978-0-7475-6300-6 |title-link=The Botany of Desire |year=2003}}</ref>

Several highly successful [[insect]] groups—especially the [[Hymenoptera]] (wasps, bees and ants) and [[Lepidoptera]] (butterflies and moths) as well as many types of [[Diptera]] (flies) and [[Coleoptera]] (beetles)—evolved in conjunction with [[flowering plant]]s during the [[Cretaceous]] (145 to 66 million years ago). The earliest bees, important pollinators today, appeared in the early Cretaceous.<ref name=Bristol>{{cite web |title=Coevolution of angiosperms and insects |url=http://palaeo.gly.bris.ac.uk/Palaeofiles/Angiosperms/coevolution.htm |publisher=University of Bristol Palaeobiology Research Group |access-date=16 January 2017 |archive-url=https://web.archive.org/web/20161220033247/http://palaeo.gly.bris.ac.uk/Palaeofiles/Angiosperms/coevolution.htm |archive-date=20 December 2016 |url-status=dead }}</ref> A group of wasps [[sister clade|sister]] to the bees evolved at the same time as flowering plants, as did the Lepidoptera.<ref name=Bristol/> Further, all the major [[clade]]s of bees first appeared between the middle and late Cretaceous, simultaneously with the adaptive radiation of the [[eudicots]] (three quarters of all angiosperms), and at the time when the angiosperms became the world's dominant plants on land.<ref name="CardinalDanforth2013">{{cite journal |last1=Cardinal |first1=Sophie |last2=Danforth |first2=Bryan N. |title=Bees diversified in the age of eudicots |journal=Proceedings of the Royal Society B |date=2013 |doi=10.1098/rspb.2012.2686 |volume=280 |issue=1755 |pages=20122686 |pmid=23363629 |pmc=3574388}}</ref>

At least three aspects of flowers appear to have coevolved between flowering plants and insects, because they involve communication between these organisms. Firstly, flowers communicate with their pollinators by scent; insects use this scent to determine how far away a flower is, to approach it, and to identify where to land and finally to feed. Secondly, flowers attract insects with patterns of stripes leading to the rewards of nectar and pollen, and colours such as blue and ultraviolet, to which their eyes are sensitive; in contrast, bird-pollinated flowers tend to be red or orange. Thirdly, flowers such as [[Ophrys|some orchids]] mimic females of particular insects, deceiving males into [[pseudocopulation]].<ref name=Bristol/><ref name=Pijl>{{cite book |first1=Leendert |last1=van der Pijl |first2=Calaway H. |last2=Dodson |title=Orchid Flowers: Their Pollination and Evolution |chapter-url=https://archive.org/details/orchidflowersthe0000pijl |chapter-url-access=registration |chapter=Chapter 11: Mimicry and Deception |publisher=[[University of Miami]] Press |location=Coral Gables |year=1966 |pages=[https://archive.org/details/orchidflowersthe0000pijl/page/129 129–141] |isbn=978-0-87024-069-0}}</ref>

The [[yucca]], ''Yucca whipplei'', is pollinated exclusively by ''Tegeticula maculata'', a [[Tegeticula|yucca moth]] that depends on the yucca for survival.<ref>{{cite web|title=Pollination Partnerships Fact Sheet |work=Flora of North America |year=2004 |first=Claire |last= Hemingway |page= 2|url=http://fna.huh.harvard.edu/files/imported/Outreach/FNAfs_yucca.pdf |quote=Yucca and Yucca Moth|archive-url = https://web.archive.org/web/20110817052152/http://fna.huh.harvard.edu/files/imported/Outreach/FNAfs_yucca.pdf |archive-date = 17 August 2011}}</ref> The moth eats the seeds of the plant, while gathering pollen. The pollen has evolved to become very sticky, and remains on the mouth parts when the moth moves to the next flower. The yucca provides a place for the moth to lay its eggs, deep within the flower away from potential predators.<ref>{{cite journal |last1=Pellmyr |first1=Olle |last2=Leebens-Mack |first2=James |title=Forty million years of mutualism: Evidence for Eocene origin of the yucca-yucca moth association |journal=PNAS |date=August 1999 |pmid=10430916 |volume=96 |issue=16 |pmc=17753 |pages=9178–9183 |bibcode=1999PNAS...96.9178P |doi=10.1073/pnas.96.16.9178 |doi-access=free }}</ref>

====Birds and bird-pollinated flowers====
{{Further|Ornithophily}}
[[File:Purple-throated carib hummingbird feeding.jpg|thumb|left|[[Purple-throated carib]] feeding from and pollinating a flower]]

[[Hummingbird]]s and [[Ornithophily|ornithophilous]] (bird-pollinated) flowers have evolved a [[mutualism (biology)|mutualistic]] relationship. The flowers have [[nectar]] suited to the birds' diet, their color suits the birds' vision and their shape fits that of the birds' bills. The blooming times of the flowers have also been found to coincide with hummingbirds' breeding seasons. The floral characteristics of ornithophilous plants vary greatly among each other compared to closely related insect-pollinated species. These flowers also tend to be more ornate, complex, and showy than their insect pollinated counterparts. It is generally agreed that plants formed coevolutionary relationships with insects first, and ornithophilous species diverged at a later time. There is not much scientific support for instances of the reverse of this divergence: from ornithophily to insect pollination. The diversity in floral phenotype in ornithophilous species, and the relative consistency observed in bee-pollinated species can be attributed to the direction of the shift in pollinator preference.<ref>{{cite journal |last1=Kay |first1=Kathleen M.|last2=Reeves |first2=Patrick A. |last3=Olmstead |first3=Richard G. |last4=Schemske|first4=Douglas W. |s2cid=2991957|title=Rapid speciation and the evolution of hummingbird pollination in neotropical Costus subgenus Costus (Costaceae): evidence from nrDNA ITS and ETS sequences |journal=American Journal of Botany |date=2005 |volume=92 |issue=11|pages=1899–1910 |doi=10.3732/ajb.92.11.1899 |pmid=21646107|doi-access= }}</ref>

Flowers have converged to take advantage of similar birds.<ref name="Brown">{{cite journal |last1=Brown |first1=James H. |last2=Kodric-Brown |first2=Astrid |title=Convergence, Competition, and Mimicry in a Temperate Community of Hummingbird-Pollinated Flowers |s2cid=53604204 |journal=Ecology |year=1979 |volume=60 |issue=5 |pages=1022–1035 |doi=10.2307/1936870|jstor=1936870|bibcode=1979Ecol...60.1022B }}</ref> Flowers compete for pollinators, and adaptations reduce unfavourable effects of this competition. The fact that birds can fly during inclement weather makes them more efficient pollinators where bees and other insects would be inactive. Ornithophily may have arisen for this reason in isolated environments with poor insect colonization or areas with plants which flower in the winter.<ref name="Brown"/><ref>{{cite journal |last1=Cronk |first1=Quentin |last2=Ojeda |first2=Isidro |title=Bird-pollinated flowers in an evolutionary and molecular context |journal=Journal of Experimental Botany |date=2008 |volume=59 |issue=4 |pages=715–727 |doi=10.1093/jxb/ern009|pmid=18326865|doi-access=free }}</ref> Bird-pollinated flowers usually have higher volumes of nectar and higher sugar production than those pollinated by insects.<ref name="Stiles">{{cite journal |last=Stiles |first=F. Gary |title=Geographical Aspects of Bird Flower Coevolution, with Particular Reference to Central America |journal=Annals of the Missouri Botanical Garden |year=1981 |volume=68 |issue=2 |pages=323–351 |doi=10.2307/2398801 |jstor=2398801 |bibcode=1981AnMBG..68..323S |s2cid=87692272 |url=https://www.biodiversitylibrary.org/part/38387 }}</ref> This meets the birds' high energy requirements, the most important determinants of flower choice.<ref name="Stiles"/> In ''[[Mimulus]]'', an increase in red pigment in petals and flower nectar volume noticeably reduces the proportion of pollination by bees as opposed to hummingbirds; while greater flower surface area increases bee pollination. Therefore, red pigments in the flowers of ''Mimulus cardinalis'' may function primarily to discourage bee visitation.<ref>{{cite journal |last1=Schemske |first1=Douglas W. |last2=Bradshaw |first2=H.D. |title=Pollinator preference and the evolution of floral traits in monkeyflowers (''Mimulus'') |journal=Proceedings of the National Academy of Sciences |date=1999 |volume=96 |issue=21 |pages=11910–11915 |doi=10.1073/pnas.96.21.11910|pmid=10518550 |bibcode=1999PNAS...9611910S |pmc=18386|doi-access=free }}</ref> In ''[[Penstemon]]'', flower traits that discourage bee pollination may be more influential on the flowers' evolutionary change than 'pro-bird' adaptations, but adaptation 'towards' birds and 'away' from bees can happen simultaneously.<ref>{{cite journal |last1=Castellanos|first1=M. C. |last2=Wilson |first2=P. |last3=Thomson |first3=J.D. |title='Anti-bee' and 'pro-bird' changes during the evolution of hummingbird pollination in Penstemon flowers |journal=Journal of Evolutionary Biology |date=2005 |volume=17 |issue=4 |pages=876–885 |doi=10.1111/j.1420-9101.2004.00729.x |pmid=15271088|doi-access=free }}</ref> However, some flowers such as ''[[Heliconia angusta]]'' appear not to be as specifically ornithophilous as had been supposed: the species is occasionally (151 visits in 120 hours of observation) visited by ''[[Trigona]]'' stingless bees. These bees are largely pollen robbers in this case, but may also serve as pollinators.<ref>{{cite journal |last1=Stein |first1=Katharina |last2=Hensen |first2=Isabell |title=Potential Pollinators and Robbers: A Study of the Floral Visitors of Heliconia Angusta (Heliconiaceae) And Their Behaviour |journal=Journal of Pollination Ecology |date=2011 |volume=4 |issue=6 |pages=39–47|doi=10.26786/1920-7603(2011)7|doi-access=free }}</ref>

Following their respective breeding seasons, several species of hummingbirds occur at the same locations in [[North America]], and several hummingbird flowers bloom simultaneously in these habitats. These flowers have [[convergent evolution|converged]] to a common [[morphology (biology)|morphology]] and color because these are effective at attracting the birds. Different lengths and curvatures of the [[petal#Corolla|corolla]] tubes can affect the efficiency of extraction in hummingbird species in relation to differences in bill morphology. Tubular flowers force a bird to orient its bill in a particular way when probing the flower, especially when the bill and corolla are both curved. This allows the plant to place [[pollen]] on a certain part of the bird's body, permitting a variety of morphological [[co-adaptation]]s.<ref name="Stiles"/>

Ornithophilous flowers need to be conspicuous to birds.<ref name="Stiles"/> Birds have their greatest spectral sensitivity and finest hue discrimination at the red end of the [[visual spectrum]],<ref name="Stiles"/> so red is particularly conspicuous to them. Hummingbirds may also be able to see ultraviolet "colors". The prevalence of ultraviolet patterns and nectar guides in nectar-poor entomophilous (insect-pollinated) flowers warns the bird to avoid these flowers.<ref name="Stiles"/> Each of the two subfamilies of hummingbirds, the [[Phaethornithinae]] (hermits) and the [[Trochilinae]], has evolved in conjunction with a particular set of flowers. Most Phaethornithinae species are associated with large [[monocotyledon]]ous herbs, while the Trochilinae prefer [[dicotyledon]]ous plant species.<ref name="Stiles"/>
<!-- could extend examples of mutualism indefinitely - might mention fish/anemone [[cleaning symbiosis]] etc.
[[File:Common clownfish curves dnsmpl.jpg|thumb|[[Ocellaris clownfish]] and [[Heteractis magnifica|Ritter's sea anemones]] live together in a [[mutualism (biology)|mutual]] service-service symbiosis, the fish driving off butterfly fish and the anemone's tentacles protecting the fish from predators.]]
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