Allochronic speciation

{{short description|Speciation arising from change in breeding time}}

Allochronic speciation (also known as allochronic isolation, or temporal isolation) is a form of speciation (specifically ecological speciation) arising from reproductive isolation that occurs due to a change in breeding time that reduces or eliminates gene flow between two populations of a species. The term allochrony is used to describe the general ecological phenomenon of the differences in phenology that arise between two or more species—speciation caused by allochrony is effectively allochronic speciation.

Environmental changes acting on a species population or populations can drive isolation. An important form of isolation is when populations are separated, not geographically, but temporally (by time). Genetic changes (mutations) over time can cause the two populations to differ—notably in phenology (events in a species life dictated by time such as breeding seasons); exhibiting unique phenotypes (the observable characteristics or traits of an organism).

Scientists have developed models to explain how this process occurs and how it is detected in natural populations. A wealth of studies exist regarding species in allochrony, with a select few that strongly suggest species are speciating or already have speciated as a direct consequence of this mode of isolation.

Model

File:Allochronic speciation.svg

Speciation ultimately results due to the reproductive isolation between two populations. This can happen in a multitude of ways, a common mode of which is known as allopatric speciation. The geographic mode, where two species become physically isolated and unable to interbreed, allows for selection to act on both populations independently. Over time, this gives rise to a new species.{{Citation | title=Speciation | author1=Jerry A. Coyne |author1link=Jerry Coyne |author2=H. Allen Orr |author2link=H. Allen Orr | date=2004 | pages=1–545 | publisher=Sinauer Associates | isbn=0-87893-091-4 }}{{rp|86}} Allochronic speciation is a form of isolation that can involve allopatry; however, it is not required.{{rp|208}}

Allochrony can involve a number of factors that induce the formation of a new species. Organisms have evolved various reproductive strategies (e.g. semelparity and iteroparity, single or multiple reproductive cycles in a lifetime) that can result in different outcomes for allochrony. Many organisms also breed at different times of the day, different seasons in the year, and even over multiple years or decades.{{Citation|title=The role of allochrony in speciation |author=Rebecca S. Taylor and Vicki L. Friesen |journal=Molecular Ecology |year=2017 |volume=26 |issue=13 |pages=3330–3342 |doi=10.1111/mec.14126 |pmid= 28370658 |s2cid=46852358 |doi-access=free |bibcode=2017MolEc..26.3330T }} Seasonal breeding in animals is a common occurrence as well as spawning (in aquatic animals) times.{{rp|202}} In plants, breeding in regards to time could involve the receptivity of the stigma (the female part of the flower) to accepting sperm, periods of pollen release (such as in conifer trees where male cones disperse pollen relying on wind to direct pollen to female cones), or the overall timing of flowering (based on possible environmental cues such as moisture levels, soil type or quality, temperature, or photoperiod).{{rp|202–206}} Even migratory patterns can play a role, as species may become isolated due to migrating at different times and to different locations.{{Citation|title=The Role of Seasonal Migration in Population Divergence and Reproductive Isolation |first1=Sheela P. |last1=Turbek|first2=Elizabeth S.C.|last2= Scordato|first3= Rebecca J. |last3=Safran |journal=Trends in Ecology & Evolution |year=2018 |volume=33 |issue=3 |pages=164–175 |doi=10.1016/j.tree.2017.11.008 |pmid= 29289354 |url= |doi-access=free }} Climate change is considered to have a significant impact on allochrony—in particular, seasonal breeding species. Modeling changes in species breeding patterns due to climate as well as understanding the genetic mechanisms that control it has proven to be important.

Because of these many factors, slight to major changes in phenology can drive divergence between two populations. For example, a species with multiple breeding seasons in a year may shift those times depending on external conditions such as temperature or predation. In the event the populations (either allopatrically or sympatrically distributed, started breeding at different times, it would prevent members of each population from exchanging genes with one another. Over time, if genes are not exchanged, genetic differences arise in each population. If natural selection acts strongly on the two populations, they may become reproductively isolated, unable to reproduce viable, fertile offspring.{{rp|202–210}}

For allochronic speciation to be considered to have actually occurred, the model necessitates three major requirements:

Phylogenetic analysis must indicate that the two taxa in question are incipient species or clearly sister taxa.
Breeding timing is required to be genetically-based (heritable) as opposed to changeable throughout life (phenotypic plasticity.
The source of divergence can be determined to be explicitly allochrony and not the result of reinforcement or other evolutionary mechanisms.

Allochrony is thought to evolve more easily the greater the heritability of reproductive timing—that is, the greater the link between genes and the timing of reproduction—the more likely speciation will occur.{{Citation|title=Population structure attributable to reproductive time: isolation by time and adaptation by time |first1=Andrew P.|last1= Hendry|first2= Troy |last2=Day |journal=Molecular Ecology |year=2005 |volume=14 |issue=4 |pages=901–916 |doi=10.1111/j.1365-294X.2005.02480.x |pmid=15773924 |s2cid=8226535 |url= |doi-access=free |bibcode=2005MolEc..14..901H }} Allochrony can be non-genetic;{{rp|203}} however genetic factors must be involved for isolation to lead to complete reproductive isolation and subsequent speciation. The time frames involving allochrony are typically divided into three categories (prevalence in nature as well as examples are provided alongside each category):

Daily (considered to be common), examples include stony corals such as Acropora or Orbicella.
Seasonally (considered to be the most common), seasonal breeding times often coincide with winter, spring, fall, or summer; examples include salmon breeding runs such as in sockeye salmon.
Yearly (considered rarer), examples include periodical cicadas and bamboo, both of which reproduce within a scale of decades.

= Population structures =

[[File:Three-dimentional differentiation space for speciation.svg|right|thumb|upright=1.4|A three-dimensional space representing speciation with axes representing the factors involved in the process.{{Citation|title=Adaptive Speciation |last1=Dieckmann|first1= U.|last2= Doebeli |first2=M.|last3= Metz|first3= JAJ|last4= Tautz|first4= D. |date=2004 |publisher=Cambridge University Press |location=Cambridge, UK |isbn=9781107404182 |url=https://user.iiasa.ac.at/~dieckman/reprints/BookExcerpts-DieckmannEtal2004.pdf}} The temporal dimension indicates allochrony. The ecological axis correlates with adaptation by time (ABT) whereas the mating axis corresponds to isolation by time (IBT). Breeding time create a fourth dimension expressed as asynchrony in breeding as opposed to synchrony. Speciation events are indicated by the varying colored paths that are taken.

A: Absent allochrony, only geographic and mate choice cause isolation.

B: Starts with geographic separation, mate choice furthers isolation, and is completed by allochrony.

C: Starts with mate-choice differentiation followed by allochrony.

D: Mating and ecological factors accompany allochrony.]]

Other phenotypic traits are often found to co-occur with reproductive timing such as flowering number, egg-clutch sizes, reproductive lifespans, or body size—what can be defined as temporal phenotypic clines. Two explanations exist for the existence of these clines: phenotypic plasticity or phenotypic heritability (or possibly a combination of both). If plastic, the clines arise when certain phenotypic traits influence breeding time—such as reproducing at times when their traits are best suited or if conditions drive the expression of traits. If heritable, the same factors may be expressed as they are in a plastic explanation; however, gene flow limitations allow for adaptation to the specific conditions of the reproductive time. This means that, "an individual with a heritable tendency to reproduce early that instead reproduced late might express traits typical of early reproducers".

Isolation by time (IBT) is partially analogous to the concept of isolation by distance (IBD) wherein genetic differences between populations increase with spatial distance.{{cite journal|title=Isolation by Distance in Equilibrium and Non-Equilibrium Populations |author=Montgomery Slatkin |journal=Evolution |year=1993 |volume=47 |issue=1 |pages=264–279 |doi=10.2307/2410134 |pmid=28568097 |jstor=2410134}} When IBT is present in a population, the variation of natural selection during a breeding season causes adaptation by time (ABT) generating adaptive temporal variation in phenotypic traits. These two concepts are described in the following sections. Studies of salmonid fishes (involving reproductive lifespans, size at adulthood, age, energy storage, the mass of ovaries, egg sizes, number of eggs in a clutch, fecundity, and rates of development) and flowering plants (involving plant size, duration of flowing time, the number of flowers, the number of fruits, the timing of fruiting, and leaf size) have provided strong evidence of IBT leading to ABT as well as studies of yearly allochrony.

== Isolation by time ==

The concept of IBT warrants two probabilities: in the event that heritability in reproductive timing exists among populations that breed during different seasons, probability of mating will be, "inversely proportional to the difference in the heritable component of their reproductive times."{{Citation|title=Assortative mating and plant phenology: evolutionary and practical consequences |author=Gordon A. Fox |journal=Evolutionary Ecology Research |year=2003 |volume=5 |issue= |pages=1–18 |url=http://www.evolutionary-ecology.com/issues/v05n01/ccar1383.pdf }} The probability of mating can also be proportional to breeding values (phenotypic trait expressed as the trait of tis offspring) for reproductive time in the event the heritability is additive (more than one gene controls the phenotypic trait). In a population, offspring will inherit the traits for reproductive time causing a decrease in gene flow while reproductive timing differences increase.

== Adaptation by time ==

Adaptation by time is an extension of divergence due to limited gene flow between populations experiencing different selective pressures.{{Citation|title=The Ecology of Adaptive Radiation |author=Dolph Schluter |date=2000 |publisher=Oxford University Press |isbn=0198505221 }} Typically this is limited to spatial variation such as in ecological speciation; however, in allochrony, selection varies not just in space, but in reproductive time—giving rise to adaptive temporal clines in phenotypic traits that are heritable. Isolation by time effectively allows adaptive temporal clines to evolve as long as the reproductive season has selective variation. Evidence for adaptation by time demands four factors: 1) time restricts gene flow, 2) the reproductive season expresses variations in phenotypic traits, 3) temporal variation is controlled genetically (it is not plastic), and 4) temporal variation is adaptive. ABT increases, "as (i) selection on the trait increases; (ii) environmental influences on reproductive time decrease; (iii) the heritability of reproductive time increases; and (iv) the temporal distribution of reproductive activity becomes increasingly uniform."

Detecting allochrony

File:Speciation (Gene flow continuum).png, parapatric, and sympatric) can exist within this continuum, as well as other non-geographic modes.]]

Because allochronic speciation can occur in conjunction with other modes and forms of speciation, researchers must attempt to determine if the initial stages of isolation were the result of allochrony. The speciation continuum of allopatry, parapatry, and sympatry have all been implicated in studies of temporal isolation.{{rp|206}} Allochrony can also facilitate reinforcement after secondary contact. The frequency of allochronic speciation is thought to common but understudied as allochrony is widespread in nature.

Testing whether or not allochrony prevents gene flow can be difficult due to the multitude of unknown variables in wild populations and the inability to replicate and manipulate it in laboratory settings.{{rp|203}} Producing viable, and fertile offspring (or the lack thereof) is not always possible; fortunately, lake of mate tests do not necessarily indicate temporal isolation is not at play.{{rp|203}} As stated prior, one of the necessary criteria is that the species in question must be sister taxa (or demonstrably incipient). This means that accurate phylogenies are vital to determining the initial stage of a speciation event.{{rp|203}}

Despite the multitude of studies, it is not always evident whether allochrony is the sole driver of speciation or if other factors acting simultaneously are responsible. This can be more challenging when speciation has already occurred (in that the taxa in question are reproductively isolated and no longer incipient). Determining how important allochrony is as a historical cause of speciation can be tested by: 1) comparative studies that show the young pairs of sister taxa are temporally isolated and 2) testing cases of incipient species in sympatry where reproductive isolation is incomplete without temporal isolation.{{rp|206}}

Determining if allochrony is the source of divergence require a key pattern to be measured: isolation (and subsequently speciation) should correlate with a decrease in overlapping breeding times. This pattern indicates that daily allochrony is more prone to gene flow (closeness of breeding times can allow accidental intermixing of populations) while yearly allochrony is the least prone to gene flow (accidental intermixing is rare if large time frames exist between mating periods).

Examples of divergence driven by allochrony

The following table documents cases of allochronic speciation. Varying degrees of certainty exist as not all cases strongly meet the three primary criteria necessitated by allochronic speciation. Species marked with an asterisk (*) indicate stronger confidence assessed by Rebecca Taylor and Vicki Friesen (2017).

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Studies and examples of allochronic speciation events

! Species

! Description

Acropora samoensis* and other Acropora spp.*

|Japanese corals found to be reproductively isolated by the timing of their spawning.{{Citation|title=Ecological and genetic aspects of reproductive isolation by different spawning times in Acropora corals |first1=H.|last1= Fukami|first2= M. |last2=Omori|first3= K. |last3=Shimoike|first4= T. |last4=Hayashibara|first5= M. |last5=Hatta |journal=Marine Biology |year=2003 |volume=142 |issue= 4|pages=679–684 |doi=10.1007/s00227-002-1001-8 |pmid= |bibcode=2003MarBi.142..679F |s2cid=81981786 |url= }} Sympatric species populations of A. samoensis coral spawn separately in the fall and spring with spawning being a heritable, likely involving the PaxC gene.{{Citation|title=Asynchronous spawning in sympatric populations of a hard coral reveals cryptic species and ancient genetic lineages |author=Natalie L Rosser |journal=Molecular Ecology |year=2015 |volume=24 |issue=19 |pages=5006–5019 |doi=10.1111/mec.13372 |pmid=26339867 |bibcode=2015MolEc..24.5006R |s2cid=13151100 |url= }}

Montastraea annularis*, M. faveolata*, and M. franksi*

|Three related species of coral that have speciated due to the timing of their spawning.{{Citation|title=Direct evidence for reproductive isolation among the three species of the Montastraea annularis complex in Central America (Panamá and Honduras) |first1=N. |last1=Knowlton|first2= J. L.|last2= Maté|first3= H. M.|last3= Guzmán|first4= R. |last4=Rowan|first5= J. |last5=Jara |journal=Marine Biology |year=1997 |volume=127 |issue= 4|pages=705–711 |doi= 10.1007/s002270050061|pmid= |bibcode=1997MarBi.127..705K |s2cid=37997956 |url= }}

Oncorhynchus nerka*, O. gorbuscha*, and O. tshawytscha

|Yearly breeding runs of Sockeye salmon occur during two periods in the year (late and early) have caused genetic isolation of incipient populations. Salmon breeding is known to be genetic but no specific genes are known for this species.{{Citation|title=Condition dependence and adaptation-by-time: breeding date, life history, and energy allocation within a population of salmon |first1=Andrew P.|last1= Hendry|first2= Ole K.|last2= Berg|first3= Thomas P.|last3= Quinn |journal=Oikos |year=1999 |volume=85 |issue=3 |pages=499–514 |doi=10.2307/3546699 |jstor=3546699 |pmid= |bibcode=1999Oikos..85..499H |url= }}{{Citation|title=Adaptive variation in senescence: reproductive lifespan in a wild salmon population |author=Andrew P Hendry, Yolanda E Morbey, Ole K Berg, and John K Wenburg |journal=Proceedings of the Royal Society B: Biological Sciences |year=2004 |volume=271 |issue=1536 |pages=259–266 |doi=10.1098/rspb.2003.2600 |pmid=15058436 |pmc=1691593 |url= }}{{Citation|title=Bimodal run distribution in a northern population of sockeye salmon (Oncorhynchus nerka): life history and genetic analysis on a temporal scale |first1=E. K.|last1= Fillatre|first2= P. |last2=Etherton|first3=D. D.|last3= Heath |journal=Molecular Ecology |year=2003 |volume=12 |issue=7 |pages=1793–1805 |doi=10.1046/j.1365-294x.2003.01869.x |pmid=12803632 |bibcode=2003MolEc..12.1793F |s2cid=25772120 |url= }} Even and odd two-year life cycles in conjunction with seasonal breeding runs of pink salmon (O. gorbuscha) has driven genetic differentiation between the two populations.{{Citation|title=Gene differentiation in Pacific salmon (Oncorhynchus Sp.): facts and models with reference to pink salmon (O. Gorbuscha) |first1=Lev A.|last1= Zhivotovsky|first2= A. J. |last2=Gharrett|first3= A. J.|last3= McGregor|first4= M. K.|last4= Glubokovsky|first5= Marcus W.|last5= Feldman |journal=Canadian Journal of Fisheries and Aquatic Sciences |year=1994 |volume=51 |issue= |pages=223–232 |doi=10.1139/f94-308 |pmid= |url= }}{{Citation|title=Comparative phylogeography of the two pink salmon broodlines: an analysis based on a mitochondrial DNA genealogy |author=D. Churikov and A. J. Gharrett |journal=Molecular Ecology |year=2002 |volume=11 |issue=6 |pages=1077–1101 |doi=10.1046/j.1365-294x.2002.01506.x |pmid=12030984 |bibcode=2002MolEc..11.1077C |s2cid=24965183 |url= }}{{Citation|title=Temporally Isolated Lineages of Pink Salmon Reveal Unique Signatures of Selection on Distinct Pools of Standing Genetic Variation |first1=Morten T. |last1=Limborg|first2= Ryan K. |last2=Waples|first3= James E. |last3=Seeb|first4= Lisa W.|last4= Seeb |journal=Journal of Heredity |year=2014 |volume=105 |issue=6 |pages=835–845 |doi=10.1093/jhered/esu063 |pmid=25292170 |doi-access=free }}{{Citation|title= Genetic variation of return date in a population of pink salmon: a consequence of fluctuating environment and dispersive selection? |last1= Smoker|first1= WW|last2= Gharrett|first2= AJ|last3= Stekoll|first3= MS |journal=Alaska Fishery Research Bulletin |year=1998 |volume=5 |issue= |pages=46–54 |doi= |pmid= |url= }}{{Citation|title=Use of a genetic marker to examine genetic interaction among subpopulations of pink salmon (Oncorhynchus gorbuscha) |last1= Gharrett |first1=AJ|last2= Lane|first2= S|last3= McGregor|first3= AJ|last4= Taylor|first4= SG |journal=Genetica |year=2001 |volume=111 |issue= 1–3|pages=259–267 |doi= 10.1023/A:1013791314900|pmid= 11841171|s2cid= 19278664 |url= }} Breeding run times also vary across the population range of the Chinook salmon (O. tshawytscha).{{Citation|title=Evolution of temporal isolation in the wild: genetic divergence in timing of migration and breeding by introduced chinook salmon populations |last1=Quinn|first1= TP|last2= Unwin|first2= MJ|last3=Kinnison |first3=MT |journal=Evolution |year=2000 |volume=54 |issue= 4|pages=1372–1385 |doi= 10.1111/j.0014-3820.2000.tb00569.x|pmid= 11005303|s2cid=23316021 |url= }}{{Citation|title=Integration of Random Forest with population-based outlier analyses provides insight on the genomic basis and evolution of run timing in Chinook salmon (Oncorhynchus tshawytscha) |last1=Brieuc|first1= MSO|last2= Ono|first2= K|last3= Drinan|first3= DP|last4=Naish|first4= KA |journal=Molecular Ecology |year=2015 |volume=24 |issue= 11|pages=2729–2746 |doi= 10.1111/mec.13211|pmid= 25913096|bibcode=2015MolEc..24.2729B |s2cid=206182207 |url= }}

Thaumetopoea pityocampa*

|Codominance in genes is associated with the emergence time for larval stages of this moth species. Winter and summer larval populations are in the process of speciating.{{Citation|title=Establishment and expansion of a Thaumetopoea pityocampa (Den. & Schiff.) (Lep. Notodontidae) population with a shifted life cycle in a production pine forest, Central-Coastal Portugal |first1=C.|last1=Pimentel|first2= T.|last2=Calvão|first3= M.|last3=Santos|first4= C.|last4=Ferreira|first5= M.|last5=Neves|first6= J.Å.|last6=Nilsson |journal=Forest Ecology and Management |year=2006 |volume=233 |issue=1 |pages=108–115 |doi=10.1016/j.foreco.2006.06.005 |pmid= |url= }}{{Citation|title=Phenotypic divergence in reproductive traits of a moth population experiencing a phenological shift |first1=Helena M |last1=Santos|first2= Maria-Rosa|last2= Paiva|first3= Susana|last3= Rocha|first4= Carole|last4= Kerdelhué|first5= Manuela|last5= Branco |journal=Ecology and Evolution |year=2013 |volume=3 |issue=15 |pages=5098–5108 |doi=10.1002/ece3.865 |pmid= 24455139|pmc=3892371 |bibcode=2013EcoEv...3.5098S |url= }}{{Citation|title= Experimental evidence for heritable reproductive time in 2 allochronic populations of pine processionary moth |first1=Manuela|last1= Branco|first2= Maria-Rosa|last2= Paiva|first3= Helena Maria|last3= Santos|first4= Christian|last4= Burban|first5=Carole|last5= Kerdelhué |journal=Insect Science |year=2017 |volume=24 |issue=2 |pages=325–335 |doi=10.1111/1744-7917.12287 |pmid=26530538 |s2cid=9091980 |url= |doi-access=free |bibcode=2017InsSc..24..325B }}

Inurois punctigera*

|Breeding is prevented in areas where mid-winter temperatures are unsuitable for the moth species. This has given rise to late and early populations.{{Citation|title=Parallel allochronic divergence in a winter moth due to disruption of reproductive period by winter harshness |first1=Satoshi |last1=Yamamoto|first2= Teiji |last2=Sota |journal=Molecular Ecology |year=2012 |volume=21 |issue=1 |pages=174–183 |doi=10.1111/j.1365-294X.2011.05371.x |pmid=22098106 |bibcode=2012MolEc..21..174Y |s2cid=23572464 |url= }}

Pemphigus populi-transversus* and P. obesinymphae*

|The gall-forming aphids produce galls on different leaves of the same host tree species. P. populi-transversus forms galls on early spring leaves while P. obesinymphae forms them on leaves in the summer. This has led to full reproductive isolation.{{Citation|title=Phylogenetic and molecular evidence for allochronic speciation in gall-forming aphids (Pemphigus) |author=Patrick Abbot and James H Withgott |journal=Evolution |year=2004 |volume=58 |issue=3 |pages=539–553 |doi= 10.1111/j.0014-3820.2004.tb01677.x|pmid=15119438 |s2cid=25277034 |url= |doi-access=free }}

Asphondylia spp.*

|Three midge species infect the stems of Larrea tridentata, A. auripila in summer, A. resinosa in winter, and A. foliosa in spring.{{Citation|title=Adaptive radiation of gall-inducing insects within a single host-plant species |author=Jeffrey B Joy and Bernard J Crespi |journal=Evolution |year=2007 |volume=61 |issue=4 |pages=784–795 |doi=10.1111/j.1558-5646.2007.00069.x |pmid=17439611|s2cid=16864372 |doi-access=free }}

Cellana spp.*

| Inhabiting different depths within centimeters, the limpets have become reproductively isolated likely due to a combination of parapatric speciation and spawn cues (e.g. spawning according to water level.{{Citation|title=Diversification of sympatric broadcast-spawning limpets (Cellana spp.) within the Hawaiian archipelago |first1=Christopher E.|last1= Bird|first2= Brenden S.|last2= Holland|first3= Brian W |last3=Bowen|first4= Robert J|last4= Toonen |journal=Molecular Ecology |year=2011 |volume=20 |issue=10 |pages=2128–2141 |doi=10.1111/j.1365-294X.2011.05081.x |pmid=21481050|bibcode=2011MolEc..20.2128B |s2cid=23432529 }}

Hydrobates spp.*

|The petrels group has reproductively isolated (in the Azores) and incipient species (other archipelagos) caused by cool and warm breeding seasons.{{Citation|title=Speciation through temporal segregation of Madeiran storm petrel (Oceanodroma castro) populations in the Azores? |author=L. R. Monteiro |journal=Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences |year=1998 |volume=353 |issue=1371 |pages=945–953 |doi=10.1098/rstb.1998.0259 |pmid= |pmc=1692297 }}{{Citation|title=Sympatric speciation by allochrony in a seabird |first1=V. L.|last1= Friesen|first2= A. L.|last2= Smith|first3= E. |last3=Gómez-Díaz|first4= M. |last4=Bolton|first5= R. W.|last5= Furness|first6= J. |last6=González-Solís|first7=L. R.|last7= Monteiro |journal=PNAS |year=2007 |volume=104 |issue=47 |pages=18589–18594 |doi=10.1073/pnas.0700446104 |pmid= 18006662|pmc=2141821 |bibcode=2007PNAS..10418589F |url=https://www.pnas.org/content/pnas/104/47/18589.full.pdf |doi-access=free }}{{Citation|title=Monteiro's Storm-petrel Oceanodroma monteiroi: a new species from the Azores |first1=Mark|last1= Bolton|first2= Andrea L. |last2=Smith|first3= Elena |last3=Gómez-díaz|first4= Vicki L. |last4=Friesen|first5= Renata|last5= Medeiros|first6= Joël|last6= Bried|first7= Jose L.|last7= Roscales|first8= Robert W. |last8=Furness |journal=Ibis |year=2008 |volume=150 |issue=4 |pages=717–727 |doi=10.1111/j.1474-919X.2008.00854.x }}

Howea belmoreana* and H. forsteriana*

|Genetically controlled flowering times have caused (in conjunction with differing soil pH levels) the reproductive isolation of two palm species on Lord Howe Island.{{Citation|title=Sympatric speciation in palms on an oceanic island |first1=Vincent |last1=Savolainen |first2=Marie-Charlotte|last2= Anstett |first3=Christian |last3=Lexer |first4=Ian |last4=Hutton |first5=James J |last5=Clarkson|first6=Maria V |last6=Norup |first7=Martyn P|last7= Powell |first8=David |last8=Springate |first9=Nicolas|last9= Salamin|first10=William J |last10=Baker |journal=Nature |year=2006 |volume=441 |issue=7090 |pages=210–213 |doi=10.1038/nature04566 |pmid=16467788 |bibcode=2006Natur.441..210S |s2cid=867216 |url= }}

Erysiphe necator*

|Exhibits evidence of isolation due to temporal differences of its host species Vitis vinifera.{{Citation |last1=Montarry |first1=Josselin |title=Spatio-temporal distribution of Erysiphe necator genetic groups and their relationship with disease levels in vineyards |journal=European Journal of Plant Pathology |volume=123 |issue=1 |pages=61–70 |year=2009 |bibcode=2009EJPP..123...61M |citeseerx=10.1.1.511.8215 |doi=10.1007/s10658-008-9343-9 |s2cid=13114251 |last2=Cartolaro |first2=Philippe |last3=Richard-Cervera |first3=Sylvie |last4=Delmotte |first4=François}}

Magicicada spp.*

|Groups of 13- and 17-year life cycle species pairs (seven species total) of cicada emerge to reproduce separated by large time frames between breeding seasons.{{Citation|title=Reproductive character displacement and speciation in periodical cicadas, with description of new species, 13-year Magicicada neotredecem |author=D. C. Marshall and J. R. Cooley |journal=Evolution |year=2000 |volume=54 |issue=4 |pages=1313–1325 |doi=10.1111/j.0014-3820.2000.tb00564.x |pmid=11005298 |s2cid=28276015 |url= |doi-access=free |hdl=2027.42/73691 |hdl-access=free }}{{Citation|title=Genetic evidence for assortative mating between 13-year cicadas and sympatric "17-year cicadas with 13-year life cycles" provides support for allochronic speciation |first1=C. |last1=Simon|first2= J.|last2= Tang|first3= S. |last3=Dalwadi|first4= G. |last4=Staley|first5= J. |last5=Deniega|first6= T. R. |last6=Unnasch |journal=Evolution |year=2000 |volume=54 |issue=4 |pages=1326–1336 |doi=10.1111/j.0014-3820.2000.tb00565.x |pmid=11005299 |s2cid=19105047 |url= |doi-access=free }}{{Citation |author=Sota |first=Teiji |title=Independent divergence of 13- and 17-y life cycles among three periodical cicada lineages |journal=PNAS |volume=110 |issue=17 |pages=6919–6924 |year=2013 |url= |bibcode=2013PNAS..110.6919S |doi=10.1073/pnas.1220060110 |pmc=3637745 |pmid=23509294 |last2=Yamamoto |first2=Satoshi |last3=Cooley |first3=John R. |last4=Hill |first4=Kathy B. R. |last5=Simon |first5=Chris |last6=Yoshimura |first6=Jin |doi-access=free}} Only every 221 years do the 13 and 17 year cycles align where both pairs emerge simultaneously.

Antitrogus parvulus*

|Two beetle cohorts express genetic differentiation from life cycles separated by two-year intervals.{{Citation|title=Overwintering, soil distribution and phenology of Childers canegrub, Antitrogus parvulus (Coleoptera: Scarabaeidae) in Queensland sugarcane |author=D. P. Logan, P. G. Allsopp, and M. P. Zalucki |journal=Bulletin of Entomological Research |year=2003 |volume=93 |issue=4 |pages=307–314 |doi=10.1079/ber2003245 |pmid= 12908916 |url= }}

Oeneis melissa semidea*

|Two-year life cycles of the butterfly species breeding groups have caused genetic differentiation.{{Citation|title=Population genetic structure and genetic diversity of the threatened White Mountain arctic butterfly (Oeneis melissa semidea) |author=A. E. Gradish, N. Keyghobadi, and G. W. Otis |journal=Conservation Genetics |year=2015 |volume=16 |issue=5 |pages=1253–1264 |doi=10.1007/s10592-015-0736-y |pmid= |bibcode=2015ConG...16.1253G |s2cid=13307002 |url= }}

Bambusoideae*

|Bamboo undergo semelparous reproduction where they live for years before mass-flowering at once. This can happen in different years and different locations. Allochronic patches are thought to have driven the diversification of global bamboo species.{{Citation|title=Ecological Determinants of Life History Evolution of Two Indian Bamboo Species |author=Madhav Gadgil and S. Narendra Prasad |journal=Biotropica |year=1984 |volume=16 |issue=3 |pages=161–172 |doi=10.2307/2388050 |jstor=2388050 |bibcode=1984Biotr..16..161G }}{{Citation|title=Synchrony and asynchrony: observations and hypotheses for the flowering wave in a long-lived semelparous bamboo |author=Donald C. Franklin |journal=Journal of Biogeography |year=2004 |volume=31 |issue=5 |pages=773–786 |doi=10.1111/j.1365-2699.2003.01057.x |bibcode=2004JBiog..31..773F |s2cid=55279438 }}{{Citation|title=Bamboo-Dominated Forests of the Southwest Amazon: Detection, Spatial Extent, Life Cycle Length and Flowering Waves |author=Anelena L. de Carvalho, Bruce W. Nelson, Milton C. Bianchini, Daniela Plagnol, Tatiana M. Kuplich, and Douglas C. Daly |journal=PLOS ONE |year=2013 |volume=8 |issue=1 |pages= e54852|doi=10.1371/journal.pone.0054852 |pmid=23359438 |pmc=3554598 |bibcode=2013PLoSO...854852C |doi-access=free }}

Spodoptera frugiperda

|A phytophagous example of two moth larvae strains breeding on either corn or rice at different times of the night. Other causes of isolation may be acting on the species. The population in the United States appears to be speciating via allochrony;{{Citation|title=Allochronic separation versus mate choice: nonrandom patterns of mating between fall armyworm host strains |author= Schöfl G, Dill A, Heckel DG, and Groot AT |journal=American Naturalist |year=2011 |volume=177 |issue= 4|pages=470–485 |doi= 10.1086/658904|pmid= 21460569|s2cid= 12528391 |url= }}{{Citation|title=Time-shifted reproductive behaviours among fall armyworm (Noctuidae: Spodoptera frugiperda) host strains: Evidence for differing modes of inheritance |author= Schöfl G, Heckel DG, and Groot AT |journal=Journal of Evolutionary Biology |year=2009 |volume=22 |issue= 7|pages=1447–1459 |doi= 10.1111/j.1420-9101.2009.01759.x|pmid= 19467132|s2cid= 22004781 |url= |doi-access= free }} however the population in Columbia does not.{{Citation|title=Assortative mating and lack of temporality between corn and rice strains of Spodoptera frugiperda (Lepidoptera, Noctuidae) from central Colombia |author= Saldamando-Benjumea CI, Estrada-Piedrahíta K, Velásquez-Vélez MI, and Bailey RI |journal=Journal of Insect Behavior |year=2014 |volume=27 |issue= 5|pages=555–566 |doi= 10.1007/s10905-014-9451-7|pmid= |bibcode= 2014JIBeh..27..555S |s2cid= 16310075 |url= }}

Anopheles gambiae and A. coluzzii

|Controlled by circadian rhythms that stimulate mating, the mosquitos swarm at slightly different times during twilight exhibit some evifence of allochrony, though it is possible that reinforcement or microallopatric speciation is at play.{{Citation|title=Strain- and sex-specific differences in daily flight activity and the circadian clock of Anopheles gambiae mosquitoes |author= Samuel S C Rund, Samuel J Lee, Brian R Bush, and Giles E Duffield |journal=Journal of Insect Physiology |year=2012 |volume=58 |issue=12 |pages=1609–1619 |doi=10.1016/j.jinsphys.2012.09.016 |pmid= 23068991 |url= }}{{Citation |author=Sawadogo |first=Simon P |title=Differences in timing of mating swarms in sympatric populations of Anopheles coluzzii and Anopheles gambiae s.s. (formerly An. gambiae M and S molecular forms) in Burkina Faso, West Africa |journal=Parasites & Vectors |volume=6 |issue=275 |pages=275–288 |year=2013 |url= |doi=10.1186/1756-3305-6-275 |pmc=3851435 |pmid=24330578 |last2=Costantini |first2=Carlo |last3=Pennetier |first3=Cédric |last4=Diabaté |first4=Abdoulaye |last5=Gibson |first5=Gabriella |last6=Dabiré |first6=Roch K |author-link5=Gabriella Gibson |doi-access=free}}

Bactrocera tryoni and B. neohumeralis

|Only laboratory hybridization has been observed between the two Queensland fruit flies, the latter of which mates only during the day time, while the former mates only at night.{{Citation|title=The likely fate of hybrids of Bactrocera tryoni and Bactrocera neohumeralis |author=N. Pike, W. Y. S. Wang, and A. Meats |journal=Heredity |year=2003 |volume=90 |issue=5 |pages=365–370 |doi=10.1038/sj.hdy.6800253 |pmid= 12714981|s2cid=34631721 |url= |doi-access=free }}

Anastrepha bistrigata and A. striata

|The fruit flies mate during morning and afternoon respectively. Courtship behavior could also be isolating the two species.{{Citation|title=Reproductive isolation between Anastrepha bistrigata and A. striata (Diptera, Tephritidae) |author=Denise Selivon and João S. Morgante |journal=Brazilian Journal of Genetics |year=1997 |volume=20 |issue=4 |pages= 583–585|doi=10.1590/S0100-84551997000400005 |pmid= |url= |doi-access=free }}

Salmo salar

|The age at full maturation as well as genetic differentiation varies between one- and three-year Atlantic salmon (these are the years in which the young fish leave to the ocean and return to their breeding grounds).{{Citation|title=Genome-wide SNP analysis reveals a genetic basis for sea-age variation in a wild population of Atlantic salmon (Salmo salar) |author=Susan E Johnston, Panu Orell, Victoria L Pritchard, Matthew P Kent, Sigbjørn Lien, Eero Niemelä, Jaakko Erkinaro, and Craig R Primmer |journal=Molecular Ecology |year=2014 |volume=23 |issue=14 |pages=3452–3468 |doi=10.1111/mec.12832 |pmid= 24931807 |s2cid=11737380 |url= }}

Anguilla anguilla

|European eels have varying rates that they mature based on environmental factors. This creates separated breeding populations that show some genetic differentiation—notably between 2–3 year breeding intervals.{{Citation|title=Evidence for isolation by time in the European eel (Anguilla anguilla L.) |author= Maes GE, Pujolar JM, Hellemans B, and Volckaert FAM |journal=Molecular Ecology |year=2006 |volume=15 |issue= 8|pages=2095–2107 |doi= 10.1111/j.1365-294X.2006.02925.x|pmid= 16780427|bibcode= 2006MolEc..15.2095M |s2cid= 10586483 |url= }}

Cuculus canorus

|Allochrony likely plays a role in the Cuckoo bird as they depend on host species for rearing their young. Hosts lay eggs at different times, and cuckoos depend on these timeframes to replace a host bird's eggs.{{Citation|title=Isolation by time and habitat and coexistence of distinct host races of the common cuckoo |author=A P Møller, A Antonov, B G Stokke, F Fossøy, A Moksnes, E Røskaft, and F Takasu |journal=Journal of Evolutionary Biology |year=2011 |volume=24 |issue=3 |pages=676–684 |doi=10.1111/j.1420-9101.2010.02202.x |pmid= 21214656 |s2cid=24056512 |url= |doi-access=free }}

Antechinus spp.

|The marsupial mice respond strongly to photoperiodic cues and in sympatric populations, reproductively isolated species are found to breed at different times.{{Citation|title=Photoperiod as a reproductive cue in the marsupial genus Antechinus: Ecological and evolutionary consequences |author= McAllan BM, Dickman CR, and Crowther MS |journal=Biological Journal of the Linnean Society |year=2006 |volume=87 |issue= 3|pages=365–379 |doi= 10.1111/j.1095-8312.2006.00571.x|pmid= |url= |doi-access=free }}

Coregonus clupeaformis

|The lake whitefish has two known forms, normal and dwarf. They have different spawning times but may have diverged in allopatry.{{Citation|title=Genetics of speciation in lake whitefishes in the Allegash Basin |author=Kirkpatrick M, and Selander RK |journal=Evolution |year=1979 |volume=33 |issue= 1Part2|pages=478–485 |doi= 10.1111/j.1558-5646.1979.tb04700.x|pmid= 28568177|s2cid=32131280 |url= |doi-access=free }}{{Citation|title=Linkage maps of the dwarf and normal lake whitefish (Coregonus clupeaformis) species complex and their hybrids reveal the genetic architecture of population divergence |author=Rogers SM, Isabel N, and Bernatchez L |journal=Genetics |year=2007 |volume=175 |issue= 1|pages=375–398 |doi= 10.1534/genetics.106.061457|pmid= 17110497|pmc=1774998 |url= }}

Exapion ulicis and E. lemovicinum

|E. lemovicinum infects Ulex minor and U. gallii plants while E. ulicis infects U. europaeus. The timing in which they lay eggs on the plant occurs in fall and spring respectively.{{Citation|title=Plant phenology and seed predation: Interactions between gorses and weevils in Brittany (France) |author= Barat M, Tarayre M, and Atlan A |journal=Entomologia Experimentalis et Applicata |year=2007 |volume=124 |issue= 2|pages=167–176 |doi= 10.1111/j.1570-7458.2007.00565.x|pmid= |bibcode= 2007EEApp.124..167B |s2cid= 85880513 |url= }}

Meconopsis autumnalis and M. paniculata

|Himalayan poppy are a fully reproductively isolated species thought to have speciated through allochrony as they exist in sympatry and flower at different times in the season.{{Citation|title=Meconopsis autumnalis and M. manasluensis (Papaveraceae), two new species of Himalayan poppy endemic to central Nepal with sympatric congeners |author= Egan PA |journal=Phytotaxa |year= 2011|volume=20 |issue= |pages=47–56 |doi= 10.11646/phytotaxa.20.1.4|pmid= |url= |doi-access= free|hdl= 2262/56528|hdl-access= free}}

Cordia spp.

|Some of the species in the genus exhibit significant variation in flowering times.{{Citation|title=Reproductive biology of some Costa Rican Cordia species (Boraginaceae) |author=Opler PA, Baker HG, and Frankie GW |journal=Biotropica |year=1975 |volume=7 |issue= 4|pages=234–247 |doi= 10.2307/2989736|jstor=2989736 |pmid= |bibcode=1975Biotr...7..234O |url= }}

Hesperiidae

|It is thought that temporal isolation is responsible for speciation in many of the 400 skipper butterfly species studied.{{Citation|title=Diel activity and reproductive isolation in a diverse assemblage of Neotropical skippers (Lepidoptera: Hesperiidae) |author= Devries PJ, Austin GT, and Martin NH |journal=Biological Journal of the Linnean Society |year=2008 |volume=94 |issue= 4|pages=723–736 |doi= 10.1111/j.1095-8312.2008.01037.x|pmid= |url= |doi-access=free }}

Bryopsidales spp.

|The green algae reproduces by releasing gametes at different times. This is thought to have driven reproductive isolation, but it is unclear if it is genetically controlled or based purely on environmental cues.{{Citation|title=The phenology of sexual reproduction by green algae (Bryopsidales) on Caribbean coral reefs |author=Clifton K and Clifton L |journal=Journal of Phycology |year=1999 |volume=35 |issue= 1|pages=24–34 |doi= 10.1046/j.1529-8817.1999.3510024.x|pmid= |bibcode=1999JPcgy..35...24C |s2cid=83704320 |url= }}

Chilo suppressalis

|Mate timing occurs at different intervals at night as well as dependence on different host plants.{{Citation|title=Difference in the time of mating activity between host-associated populations of the rice stem borer, Chilo suppressalis (Walker) |author=Ueno H, Furukawa S, and Tsuchida K |journal=Entomological Science |year=2006 |volume=9 |issue= 3|pages=255–259 |doi= 10.1111/j.1479-8298.2006.00171.x|pmid= |s2cid=86106927 |url= }}

Prodoxus quinquepunctellus

|Host races of the moths inhabit Adam's needle and thread yucca with larval emergence occurring in conjunction with flowering time. It is thought that morphology and host-shifting contribute alongside allochrony.{{Citation|title=Rapid evolution and specialization following host colonization in a yucca moth |author=Groman JD and Pellmyr O |journal=Journal of Evolutionary Biology |year=2000 |volume=13 |issue= 2|pages=223–236 |doi= 10.1046/j.1420-9101.2000.00159.x|pmid= |s2cid=84556390 |url= |doi-access=free }}

Gryllus pennsylvanicus and G. veletis

|The spring field crickets have been described as speciating in allochrony due to their maturation timing.{{Citation|title=Allochronic speciation in field crickets, and a new species, Acheta veletis |author=Alexander RD and Bigelow RS |journal=Evolution |year=1960 |volume=14 |issue= 3|pages=334–346 |doi= 10.1111/j.1558-5646.1960.tb03095.x|pmid= |hdl=2027.42/137466 |s2cid=87867996 |url= |hdl-access=free }} However more recent studies indicate that they are not sister species.{{Citation|title=Mitochondrial DNA phylogeny of North American field crickets: perspectives on the evolution of life cycles, songs, and habitat associations |author=Harrison RG, Bogdanowicz SM, and Hall C |journal=Journal of Evolutionary Biology |year=1995 |volume=8 |issue= 2|pages=209–232 |doi= 10.1046/j.1420-9101.1995.8020209.x|pmid= |s2cid=85777010 |url= |doi-access=free }}

Haemaphysalis spp. and Dermacentor spp.

|Three Hungarian tick species in the Haemaphysalis genus exhibit mating activity in sympatry during three seasonal periods, late fall, late spring, and early spring. Two tick species in the Dermacentor genus show peak activity in fall and spring.{{Citation|title=Allochronic seasonal peak activities of Dermacentor and Haemaphysalis spp. under continental climate in Hungary |author=Hornok, S. |journal=Veterinary Parasitology |year=2009 |volume=163 |issue= 4|pages=366–369 |doi= 10.1016/j.vetpar.2009.03.048|pmid= 19410373|url= }}

Strauzia longipennis

|Genetic variation is detected in three sunflower maggot fly variants that inhabit the same host plant. Their larval emergence occurs in three distinct periods of the summer keeping them partially isolated. Experimental manipulation suggests allochrony will increase as they continue to diverge.{{Citation|title=Divergence before the host shift? Prezygotic reproductive isolation among three varieties of a specialist fly on a single host plant |author= Hippee AC, Elnes ME, Armenta JS, Condon MA, and Forbes AA |journal=Ecological Entomology |year=2016 |volume=41 |issue= 4|pages=389–399 |doi= 10.1111/een.12309|pmid= |s2cid= 87320676 |url= |doi-access= free |bibcode= 2016EcoEn..41..389H }}{{Citation|title=Genetically differentiated races and speciation-with-gene-flow in the sunflower maggot, Strauzia longipennis |author= Forbes AA, Kelly PH, Middleton KA, and Condon MA |journal=Evolutionary Ecology |year=2013 |volume=27 |issue= 5|pages=1017–1032 |doi= 10.1007/s10682-012-9622-y|pmid= |s2cid= 18472327 |url= |doi-access= free |bibcode= 2013EvEco..27.1017F }}

Enchenopa binotata complex

|The phenology of members in the treehopper species complex is correlated with their host plants—when changing host species in experiment, the treehopper egg hatching time changes promoting assortive mating.{{Citation|title=Insect phenology mediated by host-plant water relations |author= Wood TK, Olmstead KL, and Guttman SI |journal=Evolution |year=1990 |volume=44 |issue= 3|pages=629–636 |doi= 10.1111/j.1558-5646.1990.tb05943.x|pmid= 28567982|s2cid= 43689173 |url= |doi-access= free }}

Milicia excelsa

|With flowering time of the African teak thought to be genetically controlled, the population exhibits isolation.{{Citation|title=Phenological patterns in a natural population of a tropical timber tree species, Milicia excelsa (Moraceae): Evidence of isolation by time and its interaction with feeding strategies of dispersers |author=Kasso Daïnou, Eric Laurenty, Grégory Mahy, Olivier J Hardy, Yves Brostaux, Nikki Tagg, and Jean-Louis Doucet |journal=American Journal of Botany |year=2012 |volume=99 |issue= 9|pages=1453–1463 |doi=10.3732/ajb.1200147 |pmid=22912370 |url=https://bsapubs.onlinelibrary.wiley.com/doi/pdf/10.3732/ajb.1200147 }}

Asteralobia sasakii

|Two populations of Cecidomyiidae gall midges differ substantially in emergence time (with no overlap) on two different Ilex hosts.{{Citation|title=Host-associated differences in emergence pattern, reproductive behavior and life history of Asteralobia sasakii (Monzen)(Diptera: Cecidomyiidae) between populations on Ilex crenata and I. integra (Aquifoliaceae) |author=Tabuchi K, Amano H |journal=Applied Entomology and Zoology |year=2003 |volume=38 |issue= 4|pages=501–508 |doi= 10.1303/aez.2003.501|pmid= |url= |doi-access=free |bibcode=2003AppEZ..38..501T }}

Salix spp.

|The Canadian willow species are found to isolated by flowering time; three of which flower early (S. bebbiana, S. discolor, S. eriocephala, and S. petiolaris) and late (S. amygdaloides, S. exigua, and S. lucida). Hybrids are not known outside of laboratory settings and exhibit intermediate flowering times. All seven species exist in sympatric distributions.{{Citation|title=Seasonal isolation as a reproductive barrier among sympatric Salix species |author=A. Mosseler and C. S. Papadopol |journal=Canadian Journal of Botany |year=1989 |volume=67 |issue= 9|pages=2563–2570 |doi=10.1139/b89-331 |pmid= |url= }}

Juncus effusus

|Sympatric populations of genetically differentiated plants flower at different times preventing hybridization. It is unclear if speciation is occurring by allochrony as reinforcement may be a stronger explanation.{{Citation|title=Separation in flowering time contributes to the maintenance of sympatric cryptic plant lineages |author=Stefan G Michalski and Walter Durka |journal=Ecology and Evolution |year=2015 |volume=5 |issue=11 |pages=2172–2184 |doi=10.1002/ece3.1481 |pmid=26078854 |pmc=4461419 |bibcode=2015EcoEv...5.2172M |url= }}

Agrostis tenuis

|The grass species A. tenuis grows on soil contaminated with high levels of copper leached from an unused mine. Adjacent is the non-contaminated soil. The populations are evolving reproductive isolation due to differences in flowering time.{{Citation |title=Evolution in Closely Adjacent Plant Populations. IV. Barriers to Gene Flow | author=Thomas McNeilly and Janis Antonovics |journal=Heredity |year=1968 |volume=23 | issue=2 |pages=205–218 |doi=10.1038/hdy.1968.29| doi-access=free }}

Anthoxanthum odoratum

|The grass species A. odoratum grows on soil contaminated with high levels of lead and zinc leached from an unused mine. Adjacent is the non-contaminated soil. The populations are evolving reproductive isolation due to differences in flowering time.

Chironomus nuditarsis

|The non-biting midge (genus Chironomus) exhibits differences in life cycle in accordance with elevation.{{Citation|title=Microevolutionary changes in populations of Chironomus nuditarsis Str. (Keyl, 1962) (Chironomidae, Diptera) from central Caucasus |author=Polukonova NV and Karmokov MK |journal=Russian Journal of Genetics |year=2013 |volume=49 |issue= 2|pages=175–181 |doi= 10.1134/S1022795413020099|pmid= |s2cid=12200060 |url= }}

Terellia fuscicornis

|Differences in courtship behavior as well as morphology are found in populations that infect different hosts (Silybum marianumand Cynara) that bloom at different times.{{Citation|title=Terellia fuscicornis (Diptera: Tephritidae): biological and morphological adaptation on artichoke and milk thistle |author= Sayar NP, Smith CA, White IM, Knio KM |journal=Journal of Natural History |year=2009 |volume=43 |issue= 19–20|pages=1159–1181 |doi= 10.1080/00222930902807742|pmid= |bibcode= 2009JNatH..43.1159S |s2cid= 56004378 |url= }}

Ampelomyces spp.

|Genetically different strains of the mycoparasitic fungus that infects apple powdery mildew completes their lifecycle before other strains that infect other mildew hosts.{{Citation|title=Temporal isolation explains host-related genetic differentiation in a group of widespread mycoparasitic fungi |author=Levente Kiss, Alexandra Pintye, Gábor M Kovács, Tünde Jankovics, Michael C Fontaine, Nick Harvey, Xiangming Xu, Philippe C Nicot, Marc Bardin, Jacqui A Shykoff, and Tatiana Giraud |journal=Molecular Ecology |year=2011 |volume=20 |issue=7 |pages=1492–1507 |doi=10.1111/j.1365-294X.2011.05007.x |pmid=21261766 |bibcode=2011MolEc..20.1492K |s2cid=34557058 |url= https://hal.archives-ouvertes.fr/hal-02329042/file/45580_20110406104614260_2.pdf}}

Glycine max and G. soja

|Wild soybean (G. soja) and cultivated soybean (G. max) can be prevented from hybridizing by inducing asynchrony in flowering time.{{Citation|title=A new method for evaluating flowering synchrony to support the temporal isolation of genetically modified crops from their wild relatives |author=Ohigashi K, Mizuguti A, Yoshimura Y, Matsuo K, and Miwa T |journal=Journal of Plant Research |year=2014 |volume=127 |issue= 1|pages=109–117 |doi= 10.1007/s10265-013-0592-0|pmid= 24122370|bibcode=2014JPlR..127..109O |s2cid=13606001 |url= }} This study is unique in that it is not an example of allochronic speciation, but instead an experiment demonstrating that allochrony can be experimentally applied to induce isolation.

Parasitoid wasps: Rhagoletis pomonella, Rhagoletis mendax, Diachasma alloeum, Diachasmimorpha mellea, and Utetes canaliculatus

|In R. pomonella (one of the most researched, model organisms), genetic data indicates heritability of emergence and its associated flight time.{{Citation|title=Experimental evidence of genome-wide impact of ecological selection during early stages of speciation-with-gene-flow |author=Scott P Egan, Gregory J Ragland, Lauren Assour, Thomas H Q Powell, Glen R Hood, Scott Emrich, Patrik Nosil, and Jeffrey L Feder |journal=Ecology Letters |year=2015 |volume=18 |issue=8 |pages=817–825 |doi=10.1111/ele.12460 |pmid=26077935 |pmc=4744793 |url= }} In commercial blueberry fields versus wild ones, the populations of R. mendax differ in their flight periods causing a reduction in gene flow.{{Citation|title=Evolution of phenologically distinct populations of Rhagoletis mendax (Diptera: Tephritidae) in Highbush Blueberry Fields |author=Teixeira LAF and Polavarapu S |journal=Annals of the Entomological Society of America |year=2003 |volume=96 |issue= 6|pages=818–827 |doi= 10.1603/0013-8746(2003)096[0818:EOPDPO]2.0.CO;2|pmid= |s2cid=85974264 |url= |doi-access=free }} Other Rhagoletis species that host on Crataegus show similar patterns.{{Citation|title=Ecological adaptation and reproductive isolation in sympatry: Genetic and phenotypic evidence for native host races of Rhagoletis pomonella |author=Thomas H Q Powell, Andrew A Forbes, Glen R Hood, and Jeffrey L Feder |journal=Molecular Ecology |year=2014 |volume=23 |issue=3 |pages=688–704 |doi=10.1111/mec.12635 |pmid= 24351094 |bibcode=2014MolEc..23..688P |s2cid=2745741 |url= }} Cospeciation of the parasitoid wasps (D. alloeum, D. mellea, and U. canaliculatus) and their host plant apple maggot has been induced by host-shifts caused by various factors such as timing of its egg hatching, fruit smell preference, philopatry, and avoidance. The egg hatching timing factor implicates allochrony.{{Citation|title=Sequential divergence and the multiplicative origin of community diversity |author=Glen R Hood, Andrew A Forbes, Thomas H Q Powell, Scott P Egan, Gabriela Hamerlinck, James J Smith, and Jeffrey L Feder |journal=Proceedings of the National Academy of Sciences |year=2015 |volume=112 |issue=44 |pages= E5980–E5989|doi=10.1073/pnas.1424717112 |pmid= 26499247 |pmc=4640724 |bibcode=2015PNAS..112E5980H |url= |doi-access=free }}

Eurosta solidaginis

|Two populations of goldenrod gall fly differ in their emergence periods on their host plants Solidago altissima and S. gigantea by 10 to 14 days preventing hybridization and causing isolation.{{Citation|title=Genetics, experience, and host-plant preference in Eurosta solidaginis: implications for host shifts and speciation |author=Craig TP, Horner JD, and Itami JK |journal=Evolution |year=2001 |volume=55 |issue= 4|pages=773–782 |doi= 10.1554/0014-3820(2001)055[0773:GEAHPP]2.0.CO;2|pmid= 11392395|s2cid=198157171 |url= }}

Falco sparverius

|Kestrels of Idaho have both migrating and year-round residents with the year-round population nesting earlier generating assortive mating.{{Citation|title=Nesting phenology, mate choice, and genetic divergence within a partially migratory population of American Kestrels |author=Anderson AM, Novak SJ, Smith JF, Steenhof K, Heath JA |journal=The Auk |year= 2016|volume=133 |issue= |pages=99–109 |doi= 10.1642/AUK-15-129.1|pmid= |s2cid=85683278 |url= |doi-access=free }}

Sylvia atricapilla

|Some genetic differentiation exists between blackcap populations that migrate to the United Kingdom and Ireland versus those that migrate to Iberia. The birds breed in sympatry in Germany; however, the UK and Ireland populations migrate back earlier causing assortive mating. Hybrids end up with intermediate migration routes.{{Citation|title=Spatial Isolation and Temporal Variation in Fitness and Condition Facilitate Divergence in a Migratory Divide |author=Claudia Hermes, Raeann Mettler, Diego Santiago-Alarcon, Gernot Segelbacher, and H. Martin Schaefer |journal=PLOS ONE |year=2015 |volume=10 |issue=12 |pages= e0144264|doi=10.1371/journal.pone.0144264 |pmid=26656955 |pmc=4681481 |bibcode=2015PLoSO..1044264H |doi-access=free }}

Junco hyemalis hyemalis and J. h. carolinensis

|Photoperiodic cues drive earlier development of the gonads in J. h. carolinensis of whom migrate to a different region to breed while only residing sympatrically with J. h. hyemalis birds for half of the year.{{Citation|title=Reproductive allochrony in seasonally sympatric populations maintained by differential response to photoperiod: implications for population divergence and response to climate change |author=Fudickar AM, Greives TJ, Atwell JW, Stricker CA, and Ketterson ED |journal=American Naturalist |year=2016 |volume=187 |issue= 4|pages=436–446 |doi= 10.1086/685296|pmid= 27028072|s2cid=16006406 |url=https://pdfs.semanticscholar.org/2fb1/1c446f21a9c80394f0fdafe84ab071c4e5f1.pdf |archive-url=https://web.archive.org/web/20200210092417/https://pdfs.semanticscholar.org/2fb1/1c446f21a9c80394f0fdafe84ab071c4e5f1.pdf |url-status=dead |archive-date=2020-02-10 }}

Daphnia pulex and D. pulicaria

|Very limited isolation is detected between the two water flea species (D. pulicaria is within the D. pulex complex) possibly the result of reproductive timing based on photoperiodic cues.{{Citation|title=Photoperiodic response of sexual reproduction in the Daphnia pulex group is reversed in two distinct habitats |author=H-W. Deng |journal=Limnology and Oceanography |year=1997 |volume=42 |issue= 3|pages=609–611 |doi= 10.4319/lo.1997.42.3.0609|pmid= |bibcode=1997LimOc..42..609W |url= |doi-access=free }}

Tibicina

|Habitat isolation, allochrony, and allopatry were identified in various pairs of seven species and subspecies of the genus (T. Corsica Corsica, T. Corsica fairmairei, T. garricola, T haematodes, T. nigronervosa, T. quadrisignata, and T. tomentosa).{{Citation|title=Spatial and ecological isolation in cicadas: first data from Tibicina (Hemiptera: Cicadoidea) in France |author=Jérôme Sueur and Stéphane Puissant |journal=European Journal of Entomology |year=2002 |volume=99 |issue= 4|pages= 477–484|doi=10.14411/EJE.2002.063 |pmid= |s2cid=56042738 |doi-access=free }}

Kaltenbachiella japonica

|The galling aphids depend on the budding of Japanese elm to hatch. Incipient populations have arisen due to changes in the budding times of the host plant.{{Citation|title=Genetic differentiation as a result of adaptation to the phenologies of individual host trees in the galling aphid Kaltenbachiella japonica |author=Komatsu T and Akimoto S |journal=Ecological Entomology |year=1995 |volume=20 |issue= 1|pages=33–42 |doi= 10.1111/j.1365-2311.1995.tb00426.x|pmid= |bibcode=1995EcoEn..20...33K |s2cid=83596331 |url= }}

Scolioneura betuleti and S. vicina

|The leaf-mining sawflies, despite being very similar, show some evidence of divergence due to seasonal flying (fall and spring respectively).{{Citation|title=Phylogenetics and evolution of host-plant use in leaf-mining sawflies (Hymenoptera: Tenthredinidae: Heterarthrinae) |author=Leppänen SA, Altenhofer E, Liston AD, and Nyman T |journal=Molecular Phylogenetics and Evolution |year=2012 |volume=64 |issue= 2|pages=331–341 |doi= 10.1016/j.ympev.2012.04.005|pmid= 22531610|url= }}{{Citation|title=Mitochondrial DNA variation in two invasive birch leaf-mining sawflies in North America |author= MacQuarrie CJK, Langor DW, and Sperling FAH |journal=The Canadian Entomologist |year=2007 |volume=139 |issue= 4|pages=545–553 |doi= 10.4039/n06-084|pmid= |s2cid= 85614594 |url= }}

Papilio canadensis and P. glaucus

|The two butterfly species have hybridized creating a hybrid population that breeds during a different time than the parent populations. Genetic evidence indicates that genes control the timing of reproduction.{{Citation|title=Impacts of climate warming on hybrid zone movement: geographically diffuse and biologically porous 'species borders' |author=Scriber JM |journal=Insect Science |year=2011 |volume=18 |issue= 2|pages=121–159 |doi= 10.1111/j.1744-7917.2010.01367.x|pmid= |s2cid=86586378 |url= }}{{Citation|title=Allochronic isolation and incipient hybrid speciation in tiger swallowtail butterflies |author=Ording GJ, Mercader RJ, Aardema ML, and Scriber JM |journal=Oecologia |year=2010 |volume=162 |issue= 2|pages=523–531 |doi= 10.1007/s00442-009-1493-8|pmid= 19937057|bibcode=2010Oecol.162..523O |s2cid=22623508 |url= }}

Tyrannus savana

|Fork-tailed flycatcher populations are diverging due to isolation by a change in breeding times and breeding grounds as a result of a loss of migratory behavior.{{Citation|title=Speciation Associated with Shifts in Migratory Behavior in an Avian Radiation |author=Valentina Gómez-Bahamón, Roberto Márquez, Alex E.Jahn, Cristina Yumi Miyaki, Diego T. Tuero, Oscar Laverde-R, Silvia Restrepo, and Carlos Daniel Cadena |journal=Current Biology |year=2020 |volume=30 |issue=7 |pages=1312–1321 |doi=10.1016/j.cub.2020.01.064 |pmid= 32197080|s2cid=214585322 |url= |doi-access=free |hdl=11336/177388 |hdl-access=free }}

Ostrinia nubilalis

|Corn borer moth strains breed at differing times of the night are considered to be incipient, however it is unclear if allochrony is exclusively causing isolation.{{Citation|title=Laboratory hybridization and mating period studies using two pheromone strains of Ostrinia nubilalis |author=Liebherr J. and Roelofs W. |journal=Annals of the Entomological Society of America |year=1975 |volume=68 |issue=2 |pages=305–309 |doi= 10.1093/aesa/68.2.305 }} Seasonal breeding may keep North American populations isolated as the number of yearly broods (voltinism) between the two strains. Sympatric to each other, Z strain is monovoltine (having a single brood in a year) and the E strain is divoltine (having two broods in a year).{{Citation|title=Components of reproductive isolation between North American pheromone strains of the European corn borer |last1=Dopman|first1= EB|last2= Robbins|first2= PS|last3=Seaman|first3= A |journal=Evolution |year=2010 |volume=64 |issue= 4|pages=881–902 |doi=10.1111/j.1558-5646.2009.00883.x|pmid=19895559 |pmc=2857697 |s2cid=9909878 }} In Europe, there is a correlation between larval emergence time and the host plant.{{Citation|title=Genetic isolation between two sympatric host-plant race of the European corn borer, Ostrina nubilalis Hübner. I. sex pheromone, moth emergence timing, and parasitism |author=Thomas Y, Bethenod M-T, Pelozuelo L, Frérot B, and Bourguet D |journal=Evolution |year=2003 |volume=57 |issue=2 |pages=261–273 |doi=10.1111/j.0014-3820.2003.tb00261.x |pmid=12683523 |s2cid=221734366 |url=https://hal.inrae.fr/hal-02671702/file/Thomas%20et%20al.%20Evolution%202003.pdf}}

New World bird species

|In an experiment testing the Asynchrony of Seasons Hypothesis (see section below), 57 different bird species found across the New World (North and South America) were found to express increased genetic differentiation in correlation with living in areas that have asynchronous precipitation.{{Citation|title=Asynchrony of seasons: genetic differentiation associated with geographic variation in climatic seasonality and reproductive phenology |author=Ignacio Quintero, Sebastián González-Caro, Paul-Camilo Zalamea, and Carlos Daniel Cadena |journal=American Naturalist |year=2014 |volume=184 |issue=3 |pages=352–363 |doi=10.1086/677261 |pmid=25141144 |s2cid=39670263 |url= }}

= Asynchrony of Seasons Hypothesis =

A noteworthy and significant pattern in nature is that of latitudinal gradients in species diversity.{{Citation|title=Latitudinal Gradients of Biodiversity: Pattern, Process, Scale, and Synthesis |author=M.R. Willig, D.M. Kaufman, and R.D. Stevens |journal=Annual Review of Ecology, Evolution, and Systematics |year=2003 |volume=34 |issue= |pages=273–309 |doi=10.1146/annurev.ecolsys.34.012103.144032 |pmid= |url= }}{{cite journal |last1=Hillebrand |first1=H |title=On the generality of the latitudinal diversity gradient. |journal=The American Naturalist |date=February 2004 |volume=163 |issue=2 |pages=192–211 |doi=10.1086/381004 |pmid=14970922 |s2cid=9886026 |url=http://oceanrep.geomar.de/4048/1/Hillebrand_2004_Amer_nat.pdf }} where species' richness (biodiversity) increases closer to Earth's equator. It is thought that one contributing factor is that rates of speciation are higher in these regions across the planet.{{cite book |last1=Schemske |first1=Doug |editor-last1=Butlin |editor-first1=Roger K. |editor-last2=Bridle |editor-first2=Jon |editor-last3=Schluter |editor-first3= Dolph |title=Speciation and patterns of diversity |publisher=Oxford University Press |date=2009 |pages=219–239 |chapter=Biotic interactions and speciation in the tropics |isbn=9780511815683 |name-list-style=amp}} The Asynchrony of Seasons Hypothesis is proposed to be a contributing factor to higher speciation rates as it relates directly to that of allochronic speciation.{{Citation|title=Latitudinal variation in the asynchrony of seasons: implications for higher rates of population differentiation and speciation in the tropics |author=Paul R. Martin, Frances Bonier, Ignacio T. Moore, and Joshua J. Tewksbury |journal=Ideas in Ecology and Evolution |year=2009 |volume=2 |issue= |pages=9–17 |doi=10.4033/iee.2009.2.3.n |pmid= |url= |doi-access=free }} The hypothesis proposes that the pattern is a result of a lack of synchrony with seasonal variations in tropical regions.

In high-latitude regions, various taxa experience similar temperatures and solar radiation in cyclic patterns due to Earth's axial tilt—generating seasons that are not found at the equator. Because of this, populations of a species have phenologies that are generally synchronous across a range allowing for unimpeded dispersal and subsequent gene flow. This results in less divergence between populations; ultimately reducing rates of speciation (and overall biodiversity).

In contrast with this, latitudes near or at the equator (tropics) experience asynchrony in seasonal variation in that the regions receive similar amounts of solar radiation and maintain consistence temperature. What does change is precipitation patterns, as they can be sporadic, scattered, and vary over very short distances. This pattern causes asynchrony in the phenologies of species populations that can ultimately act as a temporally isolating barrier to reproduction. This prevents gene flow between populations and can drive divergence, speciation, and an increase in biodiversity.

A large scale test of the hypothesis was conducted on fifty-seven New World bird species across South, Central, and North America. The findings, using DNA, geographic and ecological distances, as well as climatic data, indicated that genetic differentiation increased in species populations where asynchrony in precipitation was present. A similar pattern was found in another study of forty-eight neotropical frogs.{{Citation|title=Allochronic Divergence Driven by Spatial Asynchrony in Precipitation in Neotropical Frogs? |author=Carlos E. Guarnizo, Paola Montoya, Ignacio Quintero, and Carlos Daniel Cadena |journal= |year= 2020|volume= |issue= |pages= |doi=10.1101/2020.05.05.079210 |pmid= |s2cid=218582518 |url= }}

References

Category:Speciation