Evolution of angiosperm seed disperser mutualisms

19 Pages·2015·0.31 MB·English

Biol.Rev.(2016),91,pp.168–186. 168
doi:10.1111/brv.12164
Evolution of angiosperm seed disperser
mutualisms: the timing of origins and their
consequences for coevolutionary interactions
between angiosperms and frugivores
∗
Ove Eriksson
DepartmentofEcology,EnvironmentandPlantSciences,StockholmUniversity,SE-10691Stockholm,Sweden
ABSTRACT
Theoriginsofinteractionsbetweenangiospermsandfruit-eatingseeddispersershaveattractedmuchattentionfollowing
a seminal paper on this topic by Tiffney (1984). This review synthesizes evidence pertaining to key events during
theevolutionofangiosperm–frugivoreinteractionsandsuggestssomeimplicationsofthisevidenceforinterpretations
of angiosperm–frugivore coevolution. The most important conclusions are: (i) the diversification of angiosperm seed
size and fleshy fruits commenced around 80million years ago (Mya). The diversity of seed sizes, fruit sizes and fruit
typespeakedintheEocenearound55to50Mya.Duringthisfirstphaseoftheinteraction,angiospermsandanimals
evolvingfrugivoryexpandedintonichespacenotpreviouslyutilizedbythesegroups,asfrugivoresandpreviouslynot
existing fruit traits appeared. From the Eocene until the present, angiosperm–frugivore interactions have occurred
within a broad frame of existing niche space, as defined by fruit traits and frugivory, motivating a separation of the
angiosperm–frugivore interactions into two phases, before and after the peak in the early Eocene. (ii) The extinct
multituberculates were probably the most important frugivores during the early radiation phase of angiosperm seeds
andfleshyfruits.Primatesandrodentsarelikelytohavebeenimportantinthelatterpartofthisfirstphase.(iii)Flying
frugivores,birdsandbats,evolvedduringthesecondphase,mainlyduringtheOligoceneandMiocene,thusexploiting
an existing diversity of fleshy fruits. (iv) A drastic climate shift around the Eocene–Oligocene boundary (around
34Mya) resulted in more semi-open woodland vegetation, creating patchily occurring food resources for frugivores.
This promoted evolution of a ‘flying frugivore niche’ exploited by birds and bats. In particular, passerines became a
dominantfrugivoregroupworldwide.(v)Fleshyfruitsevolvedatnumerousoccasionsinmanyangiospermfamilies,and
manyoftheoriginationsoffleshyfruitsoccurredwellafterthepeakintheearlyEocene.(vi)Duringperiodsassociated
withenvironmentalchangealteringcoevolutionarynetworksandopeningofnichespace,reciprocalcoevolutionmay
result in strong directional selection formative for both fruit and frugivore evolution. Further evidence is needed to
test this hypothesis. Based on the abundance of plant lineages with various forms of fleshy fruits, and the diversity of
frugivores, it is suggested that periods of rapid coevolution in angiosperms and frugivores occurred numerous times
duringthe80millionyearsofangiosperm–frugivoreevolution.
Keywords: coevolution,fleshyfruits,bats,birds,megafauna,multituberculates,primates,rodents.
CONTENTS
I. Introduction .............................................................................................. 169
II. BackgroundHypotheses .................................................................................. 169
III. Arationaleforafocusonbirds,bats,primatesandrodents(amongextantseeddispersers) .............. 171
IV. Timingoforiginandradiationoffrugivorousbirds ...................................................... 172
V. Timingoforiginandradiationoffrugivorousmammals ................................................. 174
(1) Rodents .............................................................................................. 174
* Addressforcorrespondence(Tel:[phone];E-mail:[email protected]).
BiologicalReviews91(2016)168–186©2014TheAuthors.BiologicalReviewspublishedbyJohnWiley&SonsLtdonbehalfofCambridgePhilosophicalSociety.
ThisisanopenaccessarticleunderthetermsoftheCreativeCommonsAttribution-NonCommercial-NoDerivsLicense,whichpermitsuseanddistributioninanymedium,provided
theoriginalworkisproperlycited,theuseisnon-commercialandnomodificationsoradaptationsaremade.
Coevolutionbetweenangiospermsandfrugivores 169
(2) Primates .............................................................................................. 174
(3) Bats ................................................................................................... 175
VI. Timingoforiginofangiospermfleshyfruits .............................................................. 176
VII. Discussion ................................................................................................ 178
(1) Synthesisofevidenceoftiming ....................................................................... 178
(2) Implicationsforplant–frugivorecoevolution ......................................................... 179
VIII. Conclusions .............................................................................................. 182
IX. Acknowledgements ....................................................................................... 182
X. References ................................................................................................ 182
I. INTRODUCTION interactions? As pointed out by Friis etal. (2011), studies
ontheexplosiveangiospermdiversificationofplant–animal
Thisreviewconcernsthemajortransitionsintheinteractions interactions are important for understanding the origin of
between angiosperms and vertebrate seed dispersers, modern ecosystems, and inferences on causal mechanisms
focusing on the diversification of seed and fruit traits regardingtheseinteractionsdependcriticallyoncoincidence
associated with the evolution of frugivores from the late oftiming.Asummaryofevidenceontimingofeventsrelating
Cretaceous and during the Palaeogene and Neogene. The totheangiosperm–seeddisperserinteractionshouldthusbe
main topic is seed-dispersal by animals which are attracted in order, and is the rationale behind this review. The goal
bysofttissueassociatedwiththeseeds,so-calledfleshyfruits. is to discuss these questions and provide a summary of
Thetermfleshyfruitsishereusedinabroadsense,including evidenceconcerningtheoriginsanddiversificationoffleshy
any structure enclosing seeds and surrounding them with fruits and frugivores throughout the evolutionary history
a fleshy, edible, pulp layer (Jordano, 2000), thus including of angiosperms, from their origin in the early Cretaceous.
also structures that morphologically are not parts of the An additional goal is to discuss evolutionary implications
fruit, but function in that way (e.g. a strawberry, where the of the interactions between angiosperms and animal seed
juicy part is not the fruit). Although there are suggestions dispersers,oncethesehadbecomeestablished.
that fleshy tissue surrounding seeds originally evolved as a
defence structure (Mack, 2000), most discussion on fleshy
fruits has assumed that they are functionally adapted to
II. BACKGROUNDHYPOTHESES
attract seed dispersers. The same argument has been made
for a special form of granivory (seed predation) which may
be considered as functionally similar to frugivory on fleshy Today,theinteractionsbetweenangiospermsandvertebrate
fruits.Thisiswhentheanimal,despitebeingattractedbythe seeddispersersareamongthemostprominentinterrestrial
seeditselfratherthanbyafleshytissue,byscatter-hoarding ecosystems. Fleshy-fruited plants account for 36–42% of
activelycontributestoseeddispersal.AsadvocatedbyHulme woodyspeciesintemperateforestsand22–56%inMediter-
(2002) and Vander Wall & Beck (2012), frugivory and ranean scrublands (Jordano, 2000), and 70–94% of woody
scatter-hoarding dispersal systems have much in common. speciesintropicalforests(Fleming,Breitwisch&Whitesides,
In both systems, the plants provide a nutritional reward 1987; Jordano, 2000). Taxonomically, fleshy fruits occur in
(soft juicy tissue, or seeds) for the service of seed dispersal awiderangeofplantfamilies(VanderWall&Beck,2012).
by a vertebrate. Scatter-hoarding implies that a fraction of Fruits of several angiosperm families, e.g. Icacinaceae,
seedsharvestedbytheanimalisnotconsumed,andthereby Lauraceae and Vitaceae, have a well-documented fossil
functionsasdispersedpropagules.Boththeseplant–animal recordgoingbacktotheEoceneforestsmorethan50Mya,
interactionsmaybeconsideredasmutualistic,theyincludea and for Arecaceae, Cornaceae and Menispermaceae even
rewardfortheanimalandtheypromoteseeddispersal,and to the late Cretaceous (Collinson & Hooker, 1991; Harley,
theinteractionispotentiallysubjecttocoevolution. 2006; Wang etal., 2012). Figure 1 provides an account
Vertebrate-dispersedseedsoccurredlongbeforetheorigin of the geological timescale. Scatter-hoarded fruits (mainly
of angiosperms (reviewed by Tiffney, 2004), and fleshy largenuts)arecommoninthetemperatezone,forexample
tissuesurroundingseedsoccurinforexamplecycads,Ginkgo in the Betulaceae, Fagaceae and Juglandaceae (Vander
spp., Gnetales and several groups of conifers (Friis, Crane Wall & Beck, 2012), but are also important in the tropics,
& Pedersen, 2011). However, the origins of interactions particularlyinneotropicalforests(Forgetetal.,2002).
between angiosperms, specifically, and fruit-eating seed Tiffney (1984) presented data on fruit and seed size
dispersershaveattractedspecialattentionfollowingaseminal throughout angiosperm evolution that constitutes the basis
paper on this topic by Tiffney (1984). A crucial question for most accounts on coevolution between plants and
for interpreting these origins is the timing of the events. frugivores (e.g. Wing & Tiffney, 1987b; Sussman, 1991;
When did seed size start to diverge in angiosperms? When Wing&Boucher,1998;Tiffney,2004;Sussman,Rasmussen
did fleshy fruits and scatter-hoarded nuts originate? Which &Raven,2013).Inhisfigure2(Tiffney,1984,p.560)seed
were the animals that may have been involved in these volume is plotted against time, from the early Cretaceous
BiologicalReviews91(2016)168–186©2014TheAuthors.BiologicalReviewspublishedbyJohnWiley&SonsLtdonbehalfofCambridgePhilosophicalSociety.
170 OveEriksson
1e5
10000
1000
100
m )3
m
e ( 10
m
u
ol
d v 1
e
e
S
0.1
0.01
0.001
1e-4
120 100 80 60 40 20
PALAEOGENE NEOGENE
PaleocenePalaeocene Eocene Oligocene Miocene Pliocene
66 56 34 23 5
QUATERNARY
e
Pleistocen Holocene
2.6 0
Age (Mya)
Fig. 1. Average and range of seed size in angiosperms since the origin of angiosperms around 130Mya. The figure is based on
Erikssonetal.(2000a),wheredetailsondatasamplingandanalysesaredescribed.Seedsizeincreasesfromaround80Myatothe
earlyEocene,whenpalaeocommunitieswiththegreatestmaximumandaverageseedsizeareclustered,followedbyaweaktendency
ofdecliningseedsize.ThegeologicaltimescalefollowsCohenetal.(2013)anddepictstheCretaceous,andthePalaeogene,Neogene
andQuaternaryepochs.
onwards. Seed size did not change much during the development of angiosperm-dominated forest systems. In a
Cretaceous and most angiosperms had rather small seeds laterreview,Tiffney(2004,p.19)stressedthat‘theradiation
thatwereabioticallydispersed.Laterstudiesonseedsizein of birds and mammals established dispersal agents scaled
relationtoangiospermphylogenyhaveconfirmedthatbasal to move organs, which, in turn, allowed larger disseminule
angiospermlineagesgenerallyhavesmallseeds(Sims,2012). size and ultimately the establishment of closed forests...’.
According to Tiffney (1984), seed size started to increase However,Wing&Tiffney(1987a,b)incorporatedalsoother
around the Cretaceous–Palaeogene (K–Pg) boundary, aspects such as generalized herbivory and competition for
approximately 66Mya. Seed size and fruit types diversified lightinsuccessivelymoreclosedvegetation.Theysuggested
drastically during the following epoch, the Palaeocene, and thatduringthemainpartoftheCretaceous,largeherbivores
peakedduringtheearlyEocene(55to50Mya).Tiffney(1984) (dinosaurs) inflicted strong disturbance on vegetation.
remarked that there was a tendency, albeit non-significant, Angiosperms were ‘r-selected’ and adapted to disturbance.
for a decline in average seed size from the Oligocene, Thusangiospermsweresmall-seededandlackedadaptation
reachingalevelthathasremaineduntilthepresent. to seed dispersers. During the late Cretaceous, some seeds
Tiffney (1984) associated the increase in seed size became dispersed by vertebrates, but it was not until after
in angiosperms with the development of angiosperm- the K–Pg boundary, when dinosaur herbivory ceased,
dominated forest communities and advocated the idea that angiosperms became ‘K-selected’ and adapted to
that angiosperms required biotic dispersal agents to attain dispersalbyfrugivores.Wing&Tiffney(1987b)suggesteda
dominance. He suggested that the coinciding radiations of complexrelationshipwherecoevolutionbetweenplantsand
birdsandmammalswereinstrumentalinallowingdispersal dispersersisinvolvedinapositivefeedbackwithvegetation
of large, animal-dispersed propagules, thus promoting the development, such that increasing seed size and increased
BiologicalReviews91(2016)168–186©2014TheAuthors.BiologicalReviewspublishedbyJohnWiley&SonsLtdonbehalfofCambridgePhilosophicalSociety.
Coevolutionbetweenangiospermsandfrugivores 171
fraction of fleshy fruits results from both coevolution and mayhavefacilitatedevolutionoffrugivoryinprimates(thus,
a closed forest vegetation structure (figure 5 in Wing & frugivorous birds would have evolved before frugivorous
Tiffney,1987b,p.201). primates). Several of the above-mentioned papers on
Eriksson, Friis & Lo¨fgren (2000a) made an additional angiosperm seed size evolution (e.g. Tiffney, 1984; Wing &
analysisofseedsizeandfruittypesinangiospermsbasedon Tiffney,1987b;Erikssonetal.,2000a,b)areinfactquitevague
fossilflorasfromtheearlyCretaceousonwards.Theirresults on the identity of the interacting animals, referring mostly
differedfromTiffney(1984)inthattheincreaseinseedsize toapoorfossilrecord.Animportantissueisthustoidentify
commenced earlier, by approximately 80Mya, during the whichgroupsofextantandextinctanimalsweremostlikely
late Cretaceous (Fig. 1). The peak in seed size and fraction involvedinangiosperm–seeddisperserinteractions.
of animal-mediated seed dispersal in Eriksson etal. (2000a)
agreed with Tiffney (1984), i.e. palaeocommunities with
the greatest maximum and average seed size cluster in the
III. ARATIONALEFORAFOCUSONBIRDS,
earlyEocene(c.55to50Mya).Thefractionofangiosperms BATS,PRIMATESANDRODENTS(AMONG
with animal-mediated seed dispersal systems increased in EXTANTSEEDDISPERSERS)
association with the increase in seed size (Eriksson etal.,
2000a;Eriksson,2008),suggestingthatfleshyfruitsstartedto
Beforesummarizingevidencerelatedtothetimingoforigin
becomemoreabundantatthesametimeasseedsizestarted
of the fleshy fruit/seed disperser interactions, one has to
toincrease.However,adetailedstudyofoneoftheearliest
decidewhichextantanimalgroupsshouldbeconsideredas
angiospermfloras(c.124Mya)showedthataboutaquarter
frugivorous. This is not a trivial problem, since fruit eating
of the fruits already at that time were fleshy (drupes and
isaverycommonphenomenon,evenamonganimalswhich
berries), although the size of the seeds and fruits was small
donothavefruitsasthemainpartoftheirdiet.Inhisreview
(Eriksson etal., 2000b). Eriksson etal. (2000a) suggested that
onthebiologyoffigs(Ficus,Moraceae),Janzen(1979,p.40)
the initial driver behind the increasing seed size in the late
posedtherhetoricalquestion‘Whoeatsfigs?’andanswered:
CretaceousandearlyTertiarywasthestructureofthevegeta-
‘Everybody.’ Figs are often considered the single most
tion.Angiosperm-dominatedtropicalforestsexpandedfrom
important genus of fleshy-fruited plants from a present-day
the late Cretaceous and reached a maximal distribution in
fruitconsumptionviewpoint.Figsmayalsobeamongthefirst
theearlyEocene(Morley,2000,2011).Intheseforests,large
plants which were domesticated by humans (Kislev, Hart-
seedswerefavouredduetocompetitionforlight.Increased
mann&Bar-Yosef,2006).Shanahanetal.(2001)concluded
selection for animal-mediated dispersal resulted from the
thattheanimalsknowntoeatfigsinclude10%oftheworld’s
increased seed size. The increasingly common food source
birdspeciesand6%oftheworld’smammals.Themajorfig
provided by fruits led to new animal groups exploiting this eatersamongbirdsarefruitpigeons,parrotsandpasserines,
newfoodsource,andplantswerefavouredbyseed-dispersing andthemajorfig-eatersamongmammalsarebats,primates
animals which were capable of transporting large seeds. In and squirrels (Shanahan etal., 2001). This list of animal
this scenario, specialized frugivores were not the drivers groups,birds,bats,primatesandrodents,providesareason-
behind the diversification of seed size and fruits types, but ablestartingpointfordiscussingmajorgroupsoffrugivores
ratheraconsequenceoftheavailabilityofanewfoodsource. intheextantfauna.Birds,batsandprimatesconstituteatrio
The early interactions between angiosperms and mostcommonlymentionedastheanimalgroupswhichhave
seed-dispersing animals have also been discussed in the fleshyfruitsastheirmainsourceofnutrition,andthusbeing
context of evolution of one of the putative disperser themajorplayersintheseeddisperserinteraction,especially
groups, the primates. Sussman (1991) and Sussman etal. in the tropics (e.g. Fleming etal., 1987; Chapman, 1995;
(2013) suggested that euprimates (‘modern’ primates), Jordano,2000;Go´mez&Verdu´,2012;Sussmanetal.,2013).
evolved during the early Eocene in a close coevolutionary Rodents should be included both because some groups
relationship with angiosperms: ‘The evolution of modern rely strongly on fleshy fruits (in a strict sense), e.g. squirrels
primates, as well as that of fruit bats and fruit-eating birds, (Shanahan etal., 2001), but also since scatter-hoarding
maybedirectlyrelatedtotheevolutionofimprovedmeans of large nuts is here considered as functionally similar to
of exploiting (...) the fruits and seeds of flowering plants.’ frugivoryoffleshyfruit,androdentsplayanimportantrole
(Sussmanetal.,2013,p.101). inscatter-hoarding(VanderWall&Beck,2012).
The implications of the timing of the diversification of This restricted list of animal groups should not be seen
seed size and fruit types in relation to various suggested as downgrading the occurrence, and at least locally, the
seed-dispersing animals is still an open question. For importance of frugivory involving also other groups of
example,primatesmaynothavebeenanimportantcoevo- animals, for example elephants (e.g. Chapman, Chapman
lutionary agent for the initial angiosperm diversification of &Wrangham,1992;Nchanji&Plumptre,2003),carnivores
seeds and fruits, since this took place considerably earlier (e.g. Willson, 1993; Motta-Junior & Martins, 2002), and
than the radiation of primates. A similar discrepancy in oppossums, kangaroos, lemurs, ungulates, reptiles and fish
timing has been noted for other frugivores, such as birds (Jordano, 2000; Herrera, 2002), or in geologically recent
and bats (Eriksson, 2008; Fleming & Kress, 2011). Fleming times,membersofthenow-extinct‘megafauna’(e.g.Donatti
&Kress(2011)evensuggestedthatevolutionof‘bird-fruits’ etal., 2007; Guimara˜es, Galetti & Jordano, 2008; Hansen
BiologicalReviews91(2016)168–186©2014TheAuthors.BiologicalReviewspublishedbyJohnWiley&SonsLtdonbehalfofCambridgePhilosophicalSociety.
172 OveEriksson
&Galetti,2009).Thus,frugivoryshouldbedescribedasan small and probably arboreal (Padian & Chiappe, 1998;
interaction between a large number of plant species and a Chiappe & Dyke, 2002). Not very much can be concluded
diversearrayofanimals. abouttheirfeedinghabits,althoughitseemslikelythatsome
We will return to the interactions involving the Pleis- included seeds and fruits in their diet. There is some direct
tocene megafauna in Section VII, and here focus on the evidencesuggestinggranivoryinbirdsfromtheCretaceous.
extant animal groups suggested as most important for a Zhou & Zhang (2002) found traces of seeds in the fossil of
long-termperspectiveofplant–frugivoreinteractions:birds, an early Cretaceous bird of unknown affinity. Zheng etal.
bats, primates and rodents. However, for examination (2011) reported evidence that early Cretaceous birds had a
of timing of origin in relation to angiosperm seed and well-developed digestive system with a crop, a feature that
fruit diversification, additional qualification is needed to inmodernbirdsusuallyisassociatedwithgranivory.Among
identify focal taxa of these animals. In his list of ‘spe- modern bird orders, fossil evidence suggest a Cretaceous
cialized’ tropical frugivorous birds, Snow (1981) included origin for only a few (e.g. Anseriformes, Charadriiformes,
oilbirds (Caprimulgiformes), trogons (Trogoniformes), Gaviiformes, Procellariformes) (Padian & Chiappe, 1998),
turacos (Cuculiformes), mousebirds (Coliiformes), hornbills butthisevidencehasbeenquestioned(Dyke&vanTuinen,
(Coraciiformes), fruit pigeons (Columbiformes), and several 2004). Assuming that these bird orders really did evolve
groups of passerines (Passeriformes), e.g. barbets, cotingids, during the Cretaceous, it seems unlikely that they were
manakins, starlings, broadbills, corvids, honeybirds, birds frugivorous,basedontheirextantrepresentatives.
of paradise and toucans (now usually placed in Piciformes, Very little evidence on fossil birds is known from the
e.g.Patane´ etal.,2009).Extractingsimilarinformationfrom Palaeocene(Lindow&Dyke,2006;Mayr,2007;Dyke&Lin-
Fleming etal. (1987) confirms the list by Snow (1981), but dow, 2009). The bird groups that are found from this time
addsalsoparrots(Psittaciformes),cracids(Galliformes),and (e.g. Anseriformes, Ralliformes, Gruiformes, Strigiformes)
cassowaries (Struthioniformes). Among bats, two groups arenotlikelytohavebeenfrugivorous(e.g.Hwang,Mayr&
are mainly frugivorous, Old World fruit bats (megabats; Bolortsetseg, 2010; Mayr, Alvarenga & Clarke, 2011), and
Pteropodideae) and New World fruit bats (leaf-nosed bats; arboreal birds appear to be generally rare or even absent
Phyllostomideae).Inextantprimates,themajorityismainly (Mayr,2007).Althoughithasbeensuggestedthatthediversi-
frugivorous (Go´mez & Verdu´, 2012), qualifying use of the ficationofthecrowngroupsofmodernavianfamiliesdidnot
order primates as a whole. For scatter-hoarding animals
takeplacebeforetheOligocene(Mayr,2005),itseemsthat
the list becomes more limited, including mainly rodents
someofthegroupspotentiallyrelevantforfrugivorousinter-
and some passerine birds, particularly corvids (jays, rooks,
actionsmayhaveoriginatedintheEocene.Muchoftherele-
nutcrackers)(VanderWall&Beck,2012).
vantinformationcomesfromtheFurformationinDenmark
whichwaspreviouslyinterpretedaslatePalaeocene,buthas
laterbeenplacedasearlyEocene(Lindow&Dyke,2006).
IV. TIMINGOFORIGINANDRADIATIONOF Kristoffersen (2001) described findings of trogons
FRUGIVOROUSBIRDS (Trogoniformes)fromtheFurformationasmorphologically
quitesimilartoextantspecies,andshenotedthatsomeofthe
Theoriginandradiationof‘modernbirds’,Neornithes,has plantgenerawhosefruitsarepartofthedietofextanttrogons,
beensubjecttomuchdebate,andremainscontroversial(e.g. e.g. Ocotea (Lauraceae) and Hasseltia (Flacourtiaceae), have
Feduccia,1996,2003;Hedgesetal.,1996;Cooper&Penny, been found in the early Eocene London Clay (Collinson,
1997; Dyke & van Tuinen, 2004; Ericson etal., 2006; Eric- 1983). Several other groups of birds which include extant
son,2012;Mayr,2013).Themaindisagreementiswhether frugivores have records from the Eocene, for example
lineages of Neornithes radiated and diversified during the Caprimuligiformes, including extant oilbirds (Dyke & van
Cretaceous, which is suggested by molecular analyses, or Tuinen,2004)andColiiformes,includingextantmousebirds
after theK–Pg boundaryintheearlyPalaeogene, whichis (Lindow&Dyke,2006).Coliiformeswasparticularlydiverse
suggestedbyfossilevidence.Birdshaveoftenbeenconsidered duringtheEocene(Dyke&vanTuinen,2004;Mayr,2005)
verypoorlyrepresentedinthefossilrecord,makingconclu- but no evidence indicates whether they were frugivorous.
sionsonplant–disperserinteractionsinvolvingbirdsdifficult. Several studies describe Eocene records of Psittaciformes
ThisviewhasbeenquestionedbyBleiweiss(1998)andLin- (parrots)(Dyke&vanTuinen,2004;Mayr,2005;Lindow&
dow&Dyke(2006),suggestingthatthefossilrecordshould Dyke,2006;Waterhouseetal.,2008)buttheearliestparrots
beusefultoassessthebroadtemporalrelationshipsbetween mayhavebeenmoregeneralizedintheirfeedinghabits,and
thediversificationofseedsizeandfleshyfruitsandthediver- only later evolved specialized frugivory (Mayr, 2005). For
sification of various groups of potentially frugivorous birds. Cuculiformes (including extant turacos), and Coraciiformes
Forexample,of33recognizedordinal-levelcladesofextant (includingextanthornbills),thefossilrecordismeagre,and
Neornithes, 11 have been found from the Fur formation it seems unclear whether they existed in the Eocene (Dyke
(earlyEocene)inDenmark(Dyke&Lindow,2009). & van Tuinen, 2004; Mayr, 2005). An exception may be
The most diverse and widely distributed group of birds the insectivorous rollers (Coraciiformes), which are known
during the Cretaceous, judged from the fossil record, is the fromtheEocene(Feduccia,1996).Columbiformes(including
now extinct Enantiornithes, some of which were relatively extant fruit pigeons) are not known from fossils older than
BiologicalReviews91(2016)168–186©2014TheAuthors.BiologicalReviewspublishedbyJohnWiley&SonsLtdonbehalfofCambridgePhilosophicalSociety.
Coevolutionbetweenangiospermsandfrugivores 173
the Miocene (Dyke & van Tuinen, 2004; Mayr, 2005). theseindicationsofalatearrivaltothenorthernhemisphere,
EvidenceisequivocalforGalliformes.Eventhoughthestem recentmolecularevidencesuggestsoriginsofmajorpasserine
group mayhave occurredinthe Eocene,the crown groups lineages already in the late Cretaceous and diversification
including the frugivorous cracids evolved much later (Dyke of the clade Oscines (‘songbirds’, containing most extant
& van Tuinen, 2004; Mayr, 2005; Lindow & Dyke, 2006). frugivores)inthePalaeoceneorEocene(Ericsonetal.,2014).
Cassowaries (Struthioniformes) are not known before the However, Mayr (2013) strongly disagreed with suggestions
Pliocene(Feduccia,1996).Forthetoucans(Piciformes),their of a Cretaceous origin of passerines. He remarked that
originanddiversificationintheneotropicsisnotlikelytohave passerines have a generally uniform morphology, and thus
commencedbeforethemiddleMiocene(Patane´etal.,2009). that‘...aCretaceousdivergenceofcrowngrouppasserines
The bird order including most extant species and also wouldimplyanunprecedentedevolutionarystasisformore
the most diverse array of extant frugivores is the passerines than80millionyearsinoneofthemostspecies-richgroupof
(Passeriformes).Thephylogenyofpasserinesiscontroversial, endothermic vertebrates’ (Mayr, 2013, p. 7). Furthermore,
butitisknownthatpasserinesoccurredinAustraliaalready Mayr(2013)pointedoutthattheoldestundisputableoscine
in the early Eocene (Boles, 1995). This finding is consistent fossilsinthenorthernhemispherearefromlateOligocene.
withthehypothesisthatpasserinesoriginatedanddiversified Summarizing evidence of the origin and radiation of
inthesouthernhemisphere,andlaterdispersedtothenorth- frugivorous birds (Fig. 2) leads to the conclusion that some
ernhemisphere(Ericson,Irestedt&Johansson,2003;Barker seed- and fruit-eating birds (most likely the now extinct
etal., 2004; Jønsson etal., 2011), which would have been Enantiornithes)werepresentalreadyintheCretaceous.No
colonized during the Oligocene (Mayr & Manegold, 2004). evidence suggests that this feeding strategy was common,
NofossilofpasserinesinEuropeisolderthantheOligocene however. There is no strong evidence suggesting that there
(Dyke&vanTuinen,2004;Mayr,2005),andLindow&Dyke were‘modern’groupsoffrugivorousbirdsinthePalaeocene.
(2006)remarkedthattherichfossilbirdfaunafromtheearly A radiation of several lineages of modern groups of birds
Eocene Fur formation in Denmark would have contained took place during the Eocene, and many of these lineages
passerines, if there were any passerines present. Despite containfrugivoresintheextantfauna,forexampletrogons,
Age (Mya)
CRETACEOUS PALAEOGENE NEOGENE Q.
PalaeocenePaleocene Eocene Oligocene Miocene Pliocene
120 100 80 60 40 20 0
Birds
Enantiornithes
Trogoniformes
Caprimulgiformes
Coliiformes
Psittaciformes
Coraciiformes
Passeriformes
Columbiformes
Piciformes
Mammals
Multituberculates
Archaic ungulates
Plesiadapiforms
Rodents
Primates
Bats
Fig. 2. Time lines for frugivorous birds and mammals. The time lines show temporal occurrence of frugivory during the last
100millionyears,inmajorfrugivorousbirdandmammalgroupsforwhichthereareevidenceoffrugivorypriortothePliocene.A
dottedlineindicatesthattheevidenceisweak.
BiologicalReviews91(2016)168–186©2014TheAuthors.BiologicalReviewspublishedbyJohnWiley&SonsLtdonbehalfofCambridgePhilosophicalSociety.
174 OveEriksson
mousebirdsandparrots,butexceptfortrogonstheinference suggeststhatseedsandfruitswereanimportantpartofthe
thatthesereallywerefrugivorousatthattimeisweak.Most diet(Wilsonetal.,2012).
likely, passerines did not arrive to the northern hemisphere DuringthePalaeocene,averagebodymassinherbivores
before the Oligocene, and perhaps they replaced earlier (including also ‘archaic ungulates’) increased (Wing &
birds using frugivory niches (Harrison, 1979). Even if Tiffney,1987a;Janis,2000).Herbivoresatthistimewerenot
passerines originated earlier in the southern hemisphere, specialized folivores; this feeding habit disappeared along
theyarenotlikelytohavebeeninvolvedinplant–disperser with the dinosaurs, not to become common until later
interactions from the late Cretaceous to the Eocene in the during the Eocene (Janis, 2000). Plant reproductive parts,
northern hemisphere, from where most data on fossil seeds flowers,seedsandfruits,werelikelytohavebeenimportant
andfruitsarederived(Tiffney,1984;Erikssonetal.,2000a). componentsoftheherbivorediet.Thus,interactionsbetween
mammals and fleshy-fruited plants most likely had a long
history before the radiation of modern mammals. Figure 2
summarizesthetimingoforiginandradiationoffrugivorous
V. TIMINGOFORIGINANDRADIATIONOF mammals; a more detailed description of early frugivory in
FRUGIVOROUSMAMMALS rodents,primatesandbatsisgivenbelow.
Mammals originated in the late Triassic (c. 200Mya)
(1) Rodents
(Carroll,1997;Novacek,1999),orpossiblylaterduringthe
Jurassic (c. 166Mya) (O’Leary etal., 2013), and the earliest The stem group of rodents (and lagomorphs), Glires,
mammalsarethoughttohavebeengeneralized,small,noc- probablyoriginatedclosetotheK–Pgboundary(Asheretal.,
turnalpredatorsorscavengers.Estimatesbasedonmolecular 2005), and there are several fossil findings of Glires from
methods suggest origins of extant mammal orders during the Palaeocene (e.g. Meng etal., 2005, 2007). The rodent
the Cretaceous (e.g. Bininda-Emonds etal., 2007; Meredith lineage is believed to have evolved during the Palaeocene
etal., 2011), and there is some fossil evidence of eutherian (Gingerich, 2006; Blanga-Kanfi etal., 2009; O’Leary etal.,
mammals(includingallextantplacentalmammals)fromthe 2013), and some animals were ‘squirrel-like and arboreal’
Cretaceous (Ji etal., 2002; Goswami etal., 2011). However, (Agustí & Anto´n, 2002), thus potentially eating seeds and
recent studies based on a compilation of various data fruits. Although many extant rodents also are frugivorous,
(O’Leary etal., 2013), and most fossil evidence, is in accor- e.g.squirrels(Shanahanetal.,2001),rodentsareparticularly
dance with the long-held opinion that ‘modern’ mammal important seed dispersers due to scatter-hoarding of nuts
ordersradiatedduringthePalaeoceneaftertheK–Pgmass and large seeds (Vander Wall & Beck, 2012). A key
extinction event (e.g. Alroy, 1999; Meredith etal., 2011) or adaptation is their ever-growing incisors, making rodents
closetothePalaeocene–Eoceneboundary,possiblycausally exceptionally suited to handling hard fruits such as nuts.
relatedtothePalaeocene–Eocenethermalmaximum.This Collinson & Hooker (2000) suggested that granivory and
period of exceptional global warming is associated with hoardingbehaviourinrodentsevolvedandbecamecommon
theappearanceofprimatesandmodern‘hoofed’mammals during the late Eocene along with climate deterioration,
(PerissodactylaandArtiodactyla)(Gingerich,2006),andalso whereas rodent frugivory on soft fruits was more common
witharapidgeographicalspreadofseveralmodernmammal earlier during the Eocene. Angiosperm families producing
groups(Bowenetal.,2002;Smith,Rose&Gingerich,2006). typicallyrodent-dispersednutstoday,Betulaceae,Fagaceae
During the Cretaceous, before the radiation of modern and Juglandaceae, had rather small dry-winged fruits in
mammalorders,othermammalgroupshavebeensuggested the early Eocene and large nuts did not become abundant
as potential candidates of frugivorous seed-dispersing until the late Eocene (Collinson & Hooker, 1991, 2000), or
interactorswithangiosperms,suchasmultituberculatesand perhaps even later during the Oligocene (e.g. Daghlian &
didelphoid marsupials (Collinson & Hooker, 1991; Agustí Crepet,1983).
&Anto´n,2002).Inparticular,themultituberculates(which
went extinct in the late Eocene) are likely to have been
(2) Primates
important interactors with angiosperms. Multituberculates
radiatedprofoundlyfromaround85Mya,concerningbody The origin and early evolution of primates has long been
size and feeding habits (Wilson etal., 2012) and became controversial, and opinions diverge on the delimitation of
the most successful clade of late Cretaceous mammals primates, the timing of their origin, and the ecological
(Novacek, 1999). Average body mass approximately tripled conditions favouring characteristic features of primates
between85MyaandtheK–Pgboundary;thelargestspecies such as grasping extremities, nails instead of claws, optic
weighingupto5kg(Wilsonetal.,2012).Somespecieswere convergence,andbrainenlargement.Ithasbeensuggested
arboreal (Jenkins & Krause, 1983; Collinson & Hooker, that the ancestral primate lineage diverged during the late
1991), a life habit that has been suggested to be associated Cretaceous(Tavare´ etal.,2002;Soligo&Martin,2006;but
with longer life spans (Shattuk & Williams, 2010). The seeSilcoxetal.,2007).However,fossilevidenceofeuprimates
multituberculate radiation included adaptive shifts towards (‘modern’ primates) is not known before the early Eocene,
increasedherbivory,includingfrugivory,andtheirdentition andarecentestimateincludingmoleculardatasuggeststhat
BiologicalReviews91(2016)168–186©2014TheAuthors.BiologicalReviewspublishedbyJohnWiley&SonsLtdonbehalfofCambridgePhilosophicalSociety.
Coevolutionbetweenangiospermsandfrugivores 175
euprimates originated 55.8 to 50.3Mya, i.e. in the early two main groups, Megachiroptera, comprising the mostly
Eocene(O’Learyetal.,2013). frugivorous family Pteropodidae (megabats, or Old World
It has been considered likely that primate origin is fruit bats), and Microchiroptera, comprising the remaining
related to an arboreal habit. Developing this idea, Cartmill families,includingarangeofdifferentfeedingstrategies,for
(1974, 1992) suggested the ‘visual predation hypothesis’. example insectivory, frugivory and sanguivory (Baker etal.,
The key adaptation in the earliest primates, according to 2012). The main rationale for the separation of megabats
this hypothesis, was visually guided predation on insects from the remaining bat families is that megabats lack
in the understorey and canopy of tropical forests. An echolocation (apart from being generally bigger). However,
alternative hypothesis was suggested by Sussman (1991) acomprehensiveanalysisbasedonmoleculardata(Teeling
who argued that early primates were omnivorous, and etal., 2005) suggests that megabats are actually nested
consumed ‘small objects’ in the forest canopies, including within the other lineages of bats. This implies that either
insects, but primarily flowers, seeds and fruits. This echolocationhasevolvedatleasttwice,orithasbeenlostin
‘angiosperm–primate coevolution hypothesis’ has recently thelineagecomprisingmegabats.Basedonindirectevidence,
beenelaboratedinmoredetailbySussmanetal.(2013). thesecondalternativeseemsmostprobable(Simmons,2005;
These different opinions partly reflect a disagreement Teeling etal., 2005). The fossil record of bats has been
of how an extinct group of primates or primate-like consideredpoor(e.g.Eiting&Gunnell,2009).Nevertheless,
mammals, the Plesiadapiformes, are related to euprimates. there are several recent studies examining combined fossil
Plesiadapiforms were abundant during the Palaeocene andmolecularevidence,suggestingthatwenowhavearather
(e.g. Silcox & Williamson, 2012), and went extinct during consistent picture of when bats evolved, how the different
the Eocene. In contrast to Cartmill (1974), who did not bat lineages are related phylogenetically, and how early
consider plesiadapiforms as primates, later studies support
evolution of bats is related to the environmental conditions
that they should be included in primates (Bloch etal.,
during the Palaeogene (e.g. Simmons, 2005; Teeling etal.,
2007). Furthermore, well-preserved fossil remains of a
2005;Almeidaetal.,2009,2011;Dumontetal.,2012).
plesiadapiform from the Palaeocene indicate that grasping
Although it has been speculated that bats may have a
abilitiesevolvedbeforeorbitalconvergence(Bloch&Boyer,
Palaeocene origin (e.g. Teeling etal., 2005), bats do not
2002).Althoughnotaltogetherconclusivefordistinguishing
appear in the fossil record until the Eocene (Tabuce,
betweenthesetwohypotheses,thisfindingisnotinlinewith
Antunes & Sige´, 2009; Harrison & Hooker, 2010; Ravel
what we should expect from Cartmill’s (1974, 1992) visual
etal.,2011;Morgan&Czaplewski,2012;Smithetal.,2012).
predationhypothesis.
Fossil evidence suggests that the earliest bats were small
For the question of timing between the diversification of
and insectivorous (Baker etal., 2012; Smith etal., 2012).
frugivores and angiosperm seed sizes and animal-dispersed
The diversity of bats was high already in the early Eocene,
fleshy fruits, the disagreement on whether plesiadapiforms
suggesting a rapid diversification (Simmons, 2005; Teeling
shouldberegardedasprimatesishowevernotessential.Irre-
etal., 2005). This rapid diversification of bats has been
spectiveofwhetherplesiadapiformsshouldbeconsideredas
associated with the Palaeocene–Eocene thermal maximum
primates,theyareundoubtedlygoodcandidatesasfrugivo-
(Gingerich,2006),duringwhichinsectabundanceisthought
rousseeddispersersduringthePalaeocene.Plesiadapiforms
to have increased drastically (Currano etal., 2008). Key
hadawiderangeoffeedinghabits,includingfolivory(Boyer,
innovationssuchasapoweredflightandecholocationwere
Evans & Jernvall, 2010; Boyer, Costeur & Lipman, 2012)
instrumentalfortheradiationandsuccessofbats,exploiting
and frugivory (Bloch & Boyer, 2002; Sargis, 2002; Bloch
afeedingnichebasedoninsects(Simmons,2005).
etal.,2007;Chester&Beard,2012).Abalancedconclusion
Frugivory in bats seems to have evolved later, first in
may be that they were omnivores, but that fruits were an
Pteropodidae and then in some lineages of Phyllostomidae
important part of their diet. After the Palaeocene–Eocene
(Baker etal., 2012). Although Pteropodidae was separated
boundary,euprimatesradiated(Gingerich,2006).Basedon
from other bat lineages already in the early Eocene, the
reconstructionofdietoffossilprimatesfromtheEoceneand
crowngroupismorerecent(Almeidaetal.,2011).Diversifi-
early Oligocene, Strait (2001) concluded that the majority
cationofthecrown-groupPteropodidaehasbeenestimated
were frugivorous (e.g. Silcox, Dalmyn & Bloch, 2009),
to 38 to 24Mya (Almeida etal., 2009) and 28 to 18Mya
but the diet repertoire included also insectivory (e.g. Ni
(Teeling etal., 2005), i.e. during an interval from the late
etal., 2003). Palaeocene plesiadapiforms thus seem to have
EocenetoMiocene.TheancestralconditionofPhyllostomi-
had a range of feeding habits similar to the euprimates
daewasprobablyinsectivory(Rojasetal.,2011), anditwas
in the Eocene. It is thus possible that euprimates replaced
not until the diversification of the crown group, estimated
plesiadapiforms within a similar range of feeding niches
to have occurred during the late Oligocene–Miocene, 26
afterthePalaeocene–Eoceneboundary(Boyeretal.,2012).
to 15Mya (Teeling etal., 2005), that frugivory appeared
in some lineages. This diversification involved successive
(3) Bats
changes in skull morphology and biting performance, as
Bats constitute about 20% of extant species of mammals, adaptations to particular specialized diets (Dumont etal.,
and together with rodents they are the most diverse 2012). The subfamily Phyllostominae, including some
mammal orders. Bats have traditionally been divided into frugivorouslineages,diversifiedinthemiddleMiocene19.5
BiologicalReviews91(2016)168–186©2014TheAuthors.BiologicalReviewspublishedbyJohnWiley&SonsLtdonbehalfofCambridgePhilosophicalSociety.
176 OveEriksson
to 18.6Mya (Hoffmann, Hoofer & Baker, 2008). For one pericarpdevelopedfromtheovarywall,buttwomajortypes
genus of frugivorous phyllostomid bats, Sturnira, the initial offleshyfruitsareoftenrecognized,drupesandberries(e.g.
diversification has been estimated to have occurred in the Seymouretal.,2013).Boththeseareindehiscentandusually
late Miocene 15.9 to 12.6Mya, with divergence between syncarpous.Exceptionsoccurrarely,forexampleapocarpous
the two major extant lineages 5.5 to 3.7Mya (Velazco & berries in Apocynaceae (Simo˜es etal., 2007). Drupes are
Patterson, 2013). The suggested scenario is thus that some characterizedbyhavingfewseeds,usuallyonlyone,andthis
insectivorous lineages of phyllostomids during the Miocene seed is enclosed in a hard inner fruit layer, the endocarp.
evolved a successively more specialized frugivory, initially Berrieshaveathinoftenalmostunnoticeableendocarp,and
feeding on soft fruits and later feeding on harder and more theyusuallycontainmanyseeds,whichthenbynecessityare
fibre-richfruits(Rojasetal.,2012). smallerthanwhatisregularlythecasefordrupes.Although
there are one-seeded berries, for example in the Lauraceae
(e.g.avocado),mostextantberriescontainmanysmallseeds
VI. TIMINGOFORIGINOFANGIOSPERM (e.g. Ericaceae and Solanaceae). Nuts are morphologically
FLESHYFRUITS similartodrupes,butlackingafleshymesocarp(middlefruit
layer),thusenclosingtheseedwithinahardorleatheryfruit
wall.Ageneralconclusionisthatfleshyfruits,ifinterpreted
Angiosperm seeds were initially generally small, and
asanadaptationforattractinganimalseeddispersers,arethe
continued so from the origin of angiosperms somewhere
result of convergent evolution occurring in many different
around 130Mya and during the following approximately
50million years (Fig. 1). After this long period of stasis, plantlineages,andresultinginawidearrayofmorphologies.
seed and fruit size started to increase, commencing around Focusing on syncarpous fruits, drupes and nuts are the
80Mya,approximatelycoincidingwithageneralexpansion expected endpoints of selection acting on fruit structure to
phaseofangiosperms(Lupia,Lidgard&Crane,1999; Friis increase seed size. Due to a seed size/number trade-off, a
etal., 2011). Angiosperm-dominated tropical rainforests consequence is reduced seed number per fruit. Thus, the
expanded during the period from the late Cretaceous to major option to increase seed size is to evolve one-seeded
theglobalwarmingmaximumintheearlyEocene(Morley, drupes or nuts and enlarge them. This can be documented
2000,2011;Wangetal.,2012).Atthistime,tropicalforests in the palaeofloras during the period commencing around
extendedasfaras60◦N(Morley,2011).Theenvironmental 80Mya, but the trend only concerns drupes (large nuts did
context, from a vegetation viewpoint, is thus clear. The not become abundant before the late Eocene; Collinson &
diversificationofangiospermseedsizesandfruitstookplace Hooker,2000).Basedonfossilevidence,drupesdominated
alongwithexpandingtropicalforests. among the fleshy fruits during the expansion phase in the
Before summarizing evidence on timing of fleshy fruit late Cretaceous and early Palaeocene. Berries are rarely
origins, a few remarks on fruit evolution is useful. The documented in palaeofloras from the Cretaceous, but their
ancestralconditionforangiospermfruitsisapocarpy,i.e.free occurrence may be underestimated since the structure of
carpels,butthemajorityofextantangiospermshaveevolved berries makes them more difficult to detect in fossils.
syncarpous fruits, i.e. where the carpels are fused (Endress, Comparing the fraction of species with drupes in six
1982).Fruitsmaybedehiscent,i.e.theyopentoreleasethe palaeofloras spanning the period 87 to 63Mya (Table 1)
seeds,orindehiscent,remainingclosed,andtheymaybedry shows an increase from 5.6 to 33.3%. The corresponding
or fleshy. There are many different variants of fleshy fruits valuesforearlyEoceneflorasfromtheLondonClayduring
where the ‘fleshiness’ originates from other tissues than the the‘peakphase’ofangiospermseedandfruitsizearesimilar,
Table1. Fractionof‘species’withfruitsinterpretedasdrupesbasedonfossilevidencefrompalaeoflorasfromthelateCretaceous
to early Eocene. The floras are the same as those used in Eriksson etal. (2000a) for this period. Records of endocarps have been
interpretedasdrupes.Assumingconservatismoffruittypes,manyseedsfromtheseflorasindicatethatthetruefractionofdrupes
washigher,andalsothatberrieswerecommon,forexampleintheVitaceaeandAnnonaceae
Flora Age(Mya) %drupes N
Klikov-Schichtenfolge(1,2) 87 5.6 71
Aachen(1,3) 78 11.4 35
HorniBecva(1,4) 74 7.4 27
Walbeck(1) 70 24.6 65
Eisleben(1) 70 30.4 46
Gonna-Walkmu¨hlzII,IV(5) 58–63 33.3 36
LondonClay,HerneBay(6) 53 34.7 150
LondonClay,Bognor(6) 53 30.6 134
LondonClay,Sheppey(6) 53 33.3 327
Figurewithinparenthesesafterthenameofeachfloraisakeytoreferences:1,Knobloch(1964),Nemejc(1971),Knobloch&Mai(1983,
1984,1986);2,Knobloch(1985);3,Vangerow(1954);4,Knobloch(1977);5,Mai(1987);6,Reid&Chandler(1933),Chandler(1961).
BiologicalReviews91(2016)168–186©2014TheAuthors.BiologicalReviewspublishedbyJohnWiley&SonsLtdonbehalfofCambridgePhilosophicalSociety.
Coevolutionbetweenangiospermsandfrugivores 177
i.e. around a third of all species had drupes (Table 1). The robust.Furthermore,bothTiffney(1984)andErikssonetal.
florasusedinTable1arethesameasthoseusedinEriksson (2000a)notedaslightdecreaseinaverageseedsizeafterthe
etal. (2000a), showing a continuous size increase of seeds Eocene. This trend was weak, and should be viewed with
and fruits during this period. Berries were also common in caution.
theLondonClayfloras,butmanyofthesewereone-seeded Thefactthatafullrangeofvariationwithregardtofleshy
berries (Lauraceae), thus functionally similar to one-seeded fruits existed in the early Eocene does not mean that all
drupes.However,basedonseedsfromfamilieswhichtoday extant fleshy-fruited angiosperm lineages had at that time
possess berries, for example those fossil seeds identified as evolvedfleshyfruits.Eventhoughmanyangiospermfamilies
VitaceaeandAnnonaceae,thefractionofberriesmayhave seem to have conserved fruit traits ever since the Eocene
beenquitehigh. (Eriksson etal., 2000a), e.g. the Icacinaceae (Stull etal.,
Transformingthestructureofafruit(forexampleevolving 2012), both drupes and berries have evolved much more
a large drupe from a capsule) means losing dehiscence, recentlyinmanyangiospermlineages.Bolmgren&Eriksson
reducingtheseednumberperfruitinordertoenablelarger (2005) foundthat cladeswhere fleshyfruits originatedwere
seeds,developingafleshymesocarp,enclosingtheseedina temporally distributed over the last 70million years, and
hardendocarp,andenlargingtheseedandthefruit.Recent almost half the origins were younger than 40Mya. In the
evidence on fruit development pathways shows that the Rubiaceae, different kinds of fleshy fruits, drupes, berries,
genomicregulationofontogeneticdevelopmentofdifferent and‘Gardenia-fruits’haveevolvedindependentlyatleast12
kinds of fruit (capsules, berries, drupes) is similar (Seymour times(Bremer&Eriksson,1992).Moredetailedanalysesof
etal.,2013),suggestingthataconsistentdirectionalselection partsofthefamily(Kainulainenetal.,2010)suggestthatthe
would enable such a transformation without any need for number of origins is even higher. The divergence times of
fundamentallyalteringgeneregulationoffruitdevelopment. differenttribesintheRubiaceaehavebeenestimatedtospan
Detailed studies combining phylogeny and diversification from77.9to14.2Mya(Bremer&Eriksson,2009).Someof
withanalysesoffruitevolution,forSolanaceae(Knapp,2002; thesetribes,e.g.Coffeeae(divergencetime33.3to21.3Mya)
Sa¨rkinenetal.,2013)andMelastomataceae(Clausing,Meyer generally possess fleshy fruits. Relatively recent origins of
&Renner,2000),suggestthatchangesinfruitmorphology, fleshyfruitsarealsofoundinthetribeCondamineeae,where
bothfromdrytofleshyfruits,andamongdifferentformsof most lineages have capsules (Kainulainen etal., 2010). In
fleshyfruits,areontogenetically‘easy’.Althoughlikelytobe Melastomataceae fleshy fruits have originated at least three
muchlesscommon,thereisevidencealsofortransitionsfrom times(Clausingetal.,2000).Oneoftheselineages,including
fleshytodryfruits,forexampleinSolanceae(Knapp,2002), thegenusMedinilla,originatedanddiversifiedintheMiocene
Apocynaceae (Simo˜es etal., 2007), Ericaceae (Bush etal., (Renner,Clausing&Meyer,2001;Renner,2004).Another
2009)andAdoxaceae(Jacobs,Huysmans&Smets,2010). example of diversification of fleshy fruits is from the palm
Asindicatedbythepresenceofplantfamilieswhichtoday family(Arecaceae).Palmsareanancientfamilywithafossil
possess berries, this fruit type most likely was abundant in recordfromthelateCretaceous(Harley,2006).Mostpalms
theflorasfromtheEocene,andthesameholdsforlargenuts havefleshyfruits(drupes)dispersedbyawidearrayofmostly
(Collinson&Hooker,2000).Thus,asfarascanbeestablished mammalianandavianfrugivores(Zona&Henderson,1989).
fromfossilevidenceallthemajordimensionsoffruittypevari- Although the crown group of palms diversified in the late
ation(Seymouretal.,2013)concerningapocarpy/syncarpy, Cretaceous (Baker & Couvreur, 2013a), a drastic increase
dehiscence/indehiscence, dry/fleshy fruits, and among the in diversification rate occurred in the tribe Areceae much
latter, both the main types, berries and drupes, as well as a later, 38.1 to 23.6Mya (Baker & Couvreur, 2013b). This
fullseedsizerange(inrelationtopresent-dayvariation),were tribe possesses relatively small and for frugivores attractive
establishedintheearlyEocene.Althoughnotrecognizedin drupes(Baker&Couvreur,2013b).
thefossilrecord,alsothesmallestexistingangiospermseeds, The most detailed information on timing of evolution of
socalled‘dustseeds’,weremostlikelypresentintheEocene fleshy fruits within a single family is from the Solanaceae
(Eriksson&Kainulainen,2011).This‘peak’ofseedandfruit (Knapp, 2002; Sa¨rkinen etal., 2013). This family comprises
sizediversificationisthusnotonlyreferringtoaverageseed around 10000 species, of which about 2000 species belong
and fruit size (Tiffney, 1984; Eriksson etal., 2000a; Fig. 1), to the cosmopolitan genus Solanum. Capsular fruits are the
butalsotovariationinseedsizeandfruittypes. ancestral condition in the Solanaceae, and berries have
Sims (2010) examined the temporal trends in seed size originated in three separate lineages. The major lineage
described by Tiffney (1984) and Eriksson etal. (2000a) in with berries, including Solanum, branched off from its sister
relation to potential sampling errors due to the latitudinal branch (including Nicotiana) 26 to 23Mya, and initiated a
locationofpalaeofloras.Thereisastronglatitudinalgradient rapid diversification 18 to 13Mya. The other two lineages
in seed size in extant floras (Moles etal., 2007), and if withberriesarelikelytobeofamorerecentorigin.
present during the Cretaceous and Palaeogene, it could These examples, although far from exhaustive, suffice
produce a misleading picture of any temporal trend in to conclude that in many angiosperm lineages fleshy fruits
seed size. However, Sims (2010) found that the large evolved much later than the expansion phase from the
increase in seed size during the late Cretaceous and early late Cretaceous to the peak in the early Eocene. A focus
Palaeogene, reaching a peak in the early Eocene, was solely on the putative frugivores in the late Cretaceous
BiologicalReviews91(2016)168–186©2014TheAuthors.BiologicalReviewspublishedbyJohnWiley&SonsLtdonbehalfofCambridgePhilosophicalSociety.