1932

Abstract

Studies of speciation typically investigate the evolution of reproductive isolation between populations, but several other processes can serve as key steps limiting the formation of species. In particular, the probability of successful speciation can be influenced by factors that affect the frequency with which population isolates form as well as their persistence through time. We suggest that population isolation and persistence have an inherently spatial dimension that can be profitably studied using a conceptual framework drawn from metapopulation ecology. We discuss models of speciation that incorporate demographic processes and highlight the need for a broader application of phylogenetic comparative approaches to evaluate the general importance of population isolation, persistence, and reproductive isolation in speciation. We review diverse and nontraditional data sources that can be leveraged to study isolation and persistence in a comparative framework. This incorporation of spatial demographic information facilitates the integration of perspectives on speciation across disciplines and timescales.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-ecolsys-110218-024701
2019-11-02
2024-06-18
Loading full text...

Full text loading...

/deliver/fulltext/ecolsys/50/1/annurev-ecolsys-110218-024701.html?itemId=/content/journals/10.1146/annurev-ecolsys-110218-024701&mimeType=html&fmt=ahah

Literature Cited

  1. Aguilée R, Gascuel F, Lambert A, Ferriere R 2018. Clade diversification dynamics and the biotic and abiotic controls of speciation and extinction rates. Nat. Commun. 9:3013
    [Google Scholar]
  2. Allmon WD. 1992. A causal analysis of stages in allopatric speciation. Oxf. Surv. Evol. Biol. 8:219–57
    [Google Scholar]
  3. Allmon WD, Sampson SD. 2016. The stages of speciation: a stepwise framework for analysis of speciation in the fossil record. Species and Speciation in the Fossil Record WD Allmon, MM Yacobucci 121–67 Chicago: Univ. Chicago Press
    [Google Scholar]
  4. Arnold AJ, Fristrup K. 1982. The theory of evolution by natural selection: a hierarchical expansion. Paleobiology 8:113–29
    [Google Scholar]
  5. Avise JC. 2000. Phylogeography: The History and Formation of Species Cambridge, MA: Harvard Univ. Press
    [Google Scholar]
  6. Barton NH, Hewitt GM. 1985. Analysis of hybrid zones. Annu. Rev. Ecol. Syst. 16:113–48
    [Google Scholar]
  7. Birand A, Vose A, Gavrilets S 2012. Patterns of species ranges, speciation, and extinction. Am. Nat. 179:1–21
    [Google Scholar]
  8. Bolnick DI, Svanbäck R, Araújo MS, Persson L 2007. Comparative support for the niche variation hypothesis that more generalized populations are also more heterogeneous. PNAS 104:10075–79
    [Google Scholar]
  9. Burgess SC, Nickols KJ, Griesemer CD, Barnett LAK, Dedrick AG et al. 2014. Beyond connectivity: how empirical methods can quantify population persistence to improve marine protected-area design. Ecol. Appl. 24:257–70
    [Google Scholar]
  10. Cain AJ, Cook LM. 1989. Persistence and extinction in some Cepaea populations. Biol. J. Linn. Soc. 38:183–90
    [Google Scholar]
  11. Carnaval AC, Hickerson MJ, Haddad CF, Rodrigues MT, Moritz C 2009. Stability predicts genetic diversity in the Brazilian Atlantic forest hotspot. Science 323:785–89
    [Google Scholar]
  12. Carraro L, Hartikainen H, Jokela J, Bertuzzo E, Rinaldo A 2018. Estimating species distribution and abundance in river networks using environmental DNA. PNAS 115:11724–29
    [Google Scholar]
  13. Claramunt S, Derryberry EP, Remsen J Jr., Brumfield RT 2011. High dispersal ability inhibits speciation in a continental radiation of passerine birds. Proc. R. Soc. B 279:1567–74
    [Google Scholar]
  14. Cooper N, Bielby J, Thomas GH, Purvis A 2008. Macroecology and extinction risk correlates of frogs. Glob. Ecol. Biogeogr. 17:211–21
    [Google Scholar]
  15. Coyne JA, Orr HA. 2004. Speciation Sunderland, MA: Sinauer
    [Google Scholar]
  16. Coyne JA, Price TD. 2000. Little evidence for sympatric speciation in island birds. Evolution 54:2166–71
    [Google Scholar]
  17. Cunningham HR, Rissler LJ, Buckley LB, Urban MC 2016. Abiotic and biotic constraints across reptile and amphibian ranges. Ecography 39:1–8
    [Google Scholar]
  18. Cutter AD, Gray JC. 2016. Ephemeral ecological speciation and the latitudinal biodiversity gradient. Evolution 70:2171–85
    [Google Scholar]
  19. D'Aloia CC, Bogdanowicz SM, Francis RK, Majoris JE, Harrison RG, Buston PM 2015. Patterns, causes, and consequences of marine larval dispersal. PNAS 112:13940–45
    [Google Scholar]
  20. Darwin CD. 1859. On the Origin of Species by Means of Natural Selection London: J. Murray
    [Google Scholar]
  21. de Quieroz K. 2007. Species concepts and species delimitation. Syst. Biol. 56:879–86
    [Google Scholar]
  22. Dynesius M, Jansson R. 2014. Persistence of within-species lineages: a neglected control of speciation rates. Evolution 68:923–34
    [Google Scholar]
  23. Ehrlich PR, Murphy DD. 1987. Conservation lessons from long-term studies of checkerspot butterflies. Conserv. Biol. 1:122–31
    [Google Scholar]
  24. Etienne RS, Morlon H, Lambert A 2014. Estimating the duration of speciation from phylogenies. Evolution 68:2430–40
    [Google Scholar]
  25. Fink D, Auer T, Johnston A, Strimas-Mackey M, Iliff M, Kelling S 2018. eBird Status and Trends Cornell Lab of Ornithology Ithaca, NY: updated Nov. 2018. https://ebird.org/science/status-and-trends
    [Google Scholar]
  26. Futuyma DJ. 1987. On the role of species in anagenesis. Am. Nat. 130:465–73
    [Google Scholar]
  27. Gardali T, Seavy NE, DiGaudio RT, Comrack LA 2012. A climate change vulnerability assessment of California's at-risk birds. PLOS ONE 7:e29507
    [Google Scholar]
  28. Gaston KJ. 2003. The Structure and Dynamics of Geographic Ranges Oxford, UK: Oxford Univ. Press
    [Google Scholar]
  29. Gavrilets S. 2000. Waiting time to parapatric speciation. Proc. R. Soc. B 267:2483–92
    [Google Scholar]
  30. Gavrilets S. 2003. Perspective: models of speciation: What have we learned in 40 years?. Evolution 57:2197–215
    [Google Scholar]
  31. Gavrilets S, Acton R, Gravner J 2000. Dynamics of speciation and diversification in a metapopulation. Evolution 54:1493–501
    [Google Scholar]
  32. Gavrilets S, Vose A. 2005. Dynamic patterns of adaptive radiation. PNAS 102:18040–45
    [Google Scholar]
  33. Gilpin M, Hanski I 1991. Metapopulation Dynamics: Empirical and Theoretical Investigations London: Academic
    [Google Scholar]
  34. Gotelli NJ. 1991. Metapopulation models: the rescue effect, the propagule rain, and the core-satellite hypothesis. Am. Nat. 138:768–76
    [Google Scholar]
  35. Hansen TA. 1983. Modes of larval development and rates of speciation in early Tertiary neogastropods. Science 220:501–2
    [Google Scholar]
  36. Harrison S. 1991. Local extinction in a metapopulation context: an empirical evaluation. Metapopulation Dynamics: Empirical and Theoretical Investigations M Gilpin, I Hanski 73–88 London: Academic
    [Google Scholar]
  37. Harrison S, Taylor AD. 1997. Empirical evidence for metapopulation dynamics. Metapopulation Biology: Ecology, Genetics, and Evolution I Hanski, M Gilpin 27–42 San Diego, CA: Academic
    [Google Scholar]
  38. Harvey MG, Aleixo A, Ribas CC, Brumfield RT 2017a. Habitat association predicts genetic diversity and population divergence in Amazonian birds. Am. Nat. 190:631–48
    [Google Scholar]
  39. Harvey MG, Seeholzer GF, Smith BT, Rabosky DL, Cuervo AM, Brumfield RT 2017b. Positive association between population genetic differentiation and speciation rates in New World birds. PNAS 114:6328–33
    [Google Scholar]
  40. Hatfield JH, Orme CDL, Tobias JA, Banks-Leite C 2018. Trait-based indicators of bird species sensitivity to habitat loss are effective within but not across data sets. Ecol. Appl. 28:28–34
    [Google Scholar]
  41. Heaney LR. 1986. Biogeography of mammals in Southeast Asia: estimates of rates of colonization, extinction, and speciation. Biol. J. Linn. Soc. 28:127–65
    [Google Scholar]
  42. Horton KG, Van Doren BM, Stepanian PM, Hochachka WM, Farnsworth A, Kelly JF 2016. Nocturnally migrating songbirds drift when they can and compensate when they must. Sci. Rep. 6:21249
    [Google Scholar]
  43. Hubbell SH. 2001. The Unified Neutral Theory of Biodiversity and Biogeography Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  44. IUCN (Int. Union Conserv. Nat.) 2017. Guidelines for using the IUCN Red List categories and criteria. Version 13 Rep., IUCN Standards and Petitions Subcommittee Washington, DC: https://www.iucnredlist.org/resources/redlistguidelines
    [Google Scholar]
  45. Jablonski D. 1986. Larval ecology and macroevolution in marine invertebrates. Bull. Mar. Sci. 39:565–87
    [Google Scholar]
  46. Jablonski D. 1987. Heritability at the species level: analysis of geographic ranges of Cretaceous mollusks. Science 238:360–63
    [Google Scholar]
  47. Jablonski D. 2008. Species selection: theory and data. Annu. Rev. Ecol. Evol. Syst. 39:501–24
    [Google Scholar]
  48. Jablonski D, Hunt G. 2006. Larval ecology, geographic range, and species survivorship in Cretaceous mollusks: organismic versus species-level explanations. Am. Nat. 168:556–64
    [Google Scholar]
  49. Jablonski D, Lutz RA. 1983. Larval ecology of marine benthic invertebrates: paleobiological implications. Biol. Rev. 58:21–89
    [Google Scholar]
  50. Jablonski D, Roy K. 2003. Geographical range and speciation in fossil and living molluscs. Proc. R. Soc. B 270:401–6
    [Google Scholar]
  51. Jiguet F, Julliard R, Thomas CD, Dehorter O, Newson SE, Couvet D 2006. Thermal range predicts bird population resilience to extreme high temperatures. Ecol. Lett. 9:1321–30
    [Google Scholar]
  52. Kays R, Crofoot MC, Jetz W, Wikelski M 2015. Terrestrial animal tracking as an eye on life and planet. Science 348:aaa2478
    [Google Scholar]
  53. Kearney M, Porter W. 2009. Mechanistic niche modelling: combining physiological and spatial data to predict species’ ranges. Ecol. Lett. 12:334–50
    [Google Scholar]
  54. Keith DA, Akçakaya HR, Thuiller W, Midgley GF, Pearson RG et al. 2008. Predicting extinction risks under climate change: coupling stochastic population models with dynamic bioclimatic habitat models. Biol. Lett. 4:560–63
    [Google Scholar]
  55. Kirkpatrick M, Ravigné V. 2002. Speciation by natural and sexual selection: models and experiments. Am. Nat. 159:S22–35
    [Google Scholar]
  56. Kisel Y, Barraclough TG. 2010. Speciation has a spatial scale that depends on levels of gene flow. Am. Nat. 175:316–34
    [Google Scholar]
  57. Kisel Y, Moreno-Letelier AC, Bogarín D, Powell MP, Chase MW, Barraclough TG 2012. Testing the link between population genetic differentiation and clade diversification in Costa Rican orchids. Evolution 66:3035–52
    [Google Scholar]
  58. Kondrashov AS, Kondrashov FA. 1999. Interactions among quantitative traits in the course of sympatric speciation. Nature 400:351
    [Google Scholar]
  59. Krug PJ, Vendetti JE, Ellingson RA, Trowbridge CD, Hirano YM 2015. Species selection favors dispersive life histories in sea slugs, but higher per-offspring investment drives shifts to short-lived larvae. Syst. Biol. 64:983–99
    [Google Scholar]
  60. Lande R. 1993. Risks of population extinction from demographic and environmental stochasticity and random catastrophes. Am. Nat. 142:911–27
    [Google Scholar]
  61. Laurance WF, Camargo JLC, Luizão RCC, Laurance SG, Pimm SL et al. 2011. The fate of Amazonian forest fragments: a 32-year investigation. Biol. Conserv. 144:56–67
    [Google Scholar]
  62. Leibold MA, Chase JM. 2018. Metacommunity Ecology Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  63. Levin DA. 1995. Metapopulations: an arena for local speciation. J. Evol. Biol. 8:635–44
    [Google Scholar]
  64. Levins R. 1969. Some demographic and genetic consequences of environmental heterogeneity for biological control. Bull. Entomol. Soc. Amer. 15:237–40
    [Google Scholar]
  65. Li J, Huang JP, Sukumaran J, Knowles LL 2018. Microevolutionary processes impact macroevolutionary patterns. BMC Evol. Biol. 18:123
    [Google Scholar]
  66. Lorenzen ED, Nogués-Bravo D, Orlando L, Weinstock J, Binladen J et al. 2011. Species-specific responses of Late Quaternary megafauna to climate and humans. Nature 479:359–64
    [Google Scholar]
  67. Losos JB, Schluter D. 2000. Analysis of an evolutionary species–area relationship. Nature 408:847
    [Google Scholar]
  68. Lynch HJ, Naveen R, Trathan PN, Fagan WF 2012. Spatially integrated assessment reveals widespread changes in penguin populations on the Antarctic Peninsula. Ecology 93:1367–77
    [Google Scholar]
  69. MacArthur RH, Wilson EO. 1967. The Theory of Island Biogeography Princeton, NJ: Princeton Univ. Press
    [Google Scholar]
  70. Maddison WP, Midford PE, Otto SP 2007. Estimating a binary character's effect on speciation and extinction. Syst. Biol. 56:701–10
    [Google Scholar]
  71. Manel S, Schwartz MK, Luikart G, Taberlet P 2003. Landscape genetics: combining landscape ecology and population genetics. Trends Ecol. Evol. 18:189–97
    [Google Scholar]
  72. Mani G, Clarke BC. 1990. Mutational order: a major stochastic process in evolution. Proc. R. Soc. B 240:29–37
    [Google Scholar]
  73. Mayr E. 1963. Animal Species and Evolution Cambridge, MA: Belknap Press
    [Google Scholar]
  74. McPeek MA. 2008. The ecological dynamics of clade diversification and community assembly. Am. Nat. 172:E270–84
    [Google Scholar]
  75. Mitter C, Farrell B, Wiegmann B 1988. The phylogenetic study of adaptive zones: Has phytophagy promoted insect diversification?. Am. Nat. 132:107–28
    [Google Scholar]
  76. Montero-Serra I, Garrabou J, Doak DF, Figuerola L, Hereu B et al. 2018. Accounting for life-history strategies and timescales in marine restoration. Conserv. Lett. 11:e12341
    [Google Scholar]
  77. Moore RP, Robinson WD, Lovette IJ, Robinson TR 2008. Experimental evidence for extreme dispersal limitation in tropical forest birds. Ecol. Lett. 11:960–68
    [Google Scholar]
  78. Muir CD, Hahn MW. 2015. The limited contribution of reciprocal gene loss to increased speciation rates following whole-genome duplication. Am. Nat. 185:70–86
    [Google Scholar]
  79. Nee S. 2006. Birth-death models in macroevolution. Annu. Rev. Ecol. Evol. Syst. 37:1–17
    [Google Scholar]
  80. Nosil P, Flaxman SM. 2010. Conditions for mutation-order speciation. Proc. R. Soc. B 278:399–407
    [Google Scholar]
  81. Orr HA, Orr LH. 1996. Waiting for speciation: the effect of population subdivision on the time to speciation. Evolution 50:1742–49
    [Google Scholar]
  82. Orr HA, Turelli M. 2001. The evolution of postzygotic isolation: accumulating Dobzhansky-Muller incompatibilities. Evolution 55:1085–94
    [Google Scholar]
  83. Pacifici M, Foden WB, Visconti P, Watson JE, Butchart SH et al. 2015. Assessing species vulnerability to climate change. Nat. Clim. Change 5:215–24
    [Google Scholar]
  84. Panhuis TM, Butlin R, Zuk M, Tregenza T 2001. Sexual selection and speciation. Trends Ecol. Evol. 16:364–71
    [Google Scholar]
  85. Petkova D, Novembre J, Stephens M 2016. Visualizing spatial population structure with estimated effective migration surfaces. Nat. Genet. 48:94
    [Google Scholar]
  86. Phillimore AB, Freckleton RP, Orme CDL, Owens IP 2006. Ecology predicts large-scale patterns of phylogenetic diversification in birds. Am. Nat. 168:220–29
    [Google Scholar]
  87. Price TD, Hooper DM, Buchanan CD, Johansson US, Tietze DT et al. 2014. Niche filling slows the diversification of Himalayan songbirds. Nature 509:222–25
    [Google Scholar]
  88. Rabinowitz D. 1981. Seven forms of rarity. Biological Aspects of Rare Plant Conservation H Synge 205–17 Chichester, UK: Wiley and Sons
    [Google Scholar]
  89. Rabosky DL. 2016. Reproductive isolation and the causes of speciation rate variation in nature. Biol. J. Linn. Soc. 118:13–25
    [Google Scholar]
  90. Rabosky DL, Matute DR. 2013. Macroevolutionary speciation rates are decoupled from the evolution of intrinsic reproductive isolation in Drosophila and birds. PNAS 110:15354–59
    [Google Scholar]
  91. Rangel TF, Edwards NR, Holden PB, Diniz-Filho JAF, Gosling WD et al. 2018. Modeling the ecology and evolution of biodiversity: biogeographical cradles, museums, and graves. Science 361:eaar5452
    [Google Scholar]
  92. Reznick DN, Ricklefs RE. 2009. Darwin's bridge between microevolution and macroevolution. Nature 457:837
    [Google Scholar]
  93. Riginos C, Buckley YM, Blomberg SP, Treml EA 2014. Dispersal capacity predicts both population genetic structure and species richness in reef fishes. Am. Nat. 184:52–64
    [Google Scholar]
  94. Robinson JA, Brown C, Kim BY, Lohmueller KE, Wayne RK 2018. Purging of strongly deleterious mutations explains long-term persistence and absence of inbreeding depression in island foxes. Curr. Biol. 28:3487–94
    [Google Scholar]
  95. Rosenblum EB, Sarver BA, Brown JW, Des Roches S, Hardwick KM et al. 2012. Goldilocks meets Santa Rosalia: an ephemeral speciation model explains patterns of diversification across time scales. Evol. Biol. 39:255–61
    [Google Scholar]
  96. Rosindell J, Cornell SJ, Hubbell SP, Etienne RS 2010. Protracted speciation revitalizes the neutral theory of biodiversity. Ecol. Lett. 13:716–27
    [Google Scholar]
  97. Rosindell J, Phillimore AB. 2011. A unified model of island biogeography sheds light on the zone of radiation. Ecol. Lett. 14:552–60
    [Google Scholar]
  98. Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I 1998. Inbreeding and extinction in a butterfly metapopulation. Nature 392:491
    [Google Scholar]
  99. Sanderson FJ, Donald PF, Pain DJ, Burfield IJ, Van Bommel FP 2006. Long-term population declines in Afro-Palearctic migrant birds. Biol. Conserv. 131:93–105
    [Google Scholar]
  100. Schluter D. 2009. Evidence for ecological speciation and its alternative. Science 323:737–41
    [Google Scholar]
  101. Schluter D. 2016. Speciation, ecological opportunity, and latitude (American Society of Naturalists Address). Am. Nat. 187:1–18
    [Google Scholar]
  102. Seeholzer GF, Brumfield RT. 2018. Isolation by distance, not incipient ecological speciation, explains genetic differentiation in an Andean songbird (Aves: Furnariidae: Cranioleuca antisiensis, Line-cheeked Spinetail) despite near threefold body size change across an environmental gradient. Mol. Ecol. 27:279–96
    [Google Scholar]
  103. Shanks AL. 2009. Pelagic larval duration and dispersal distance revisited. Biol. Bull. 216:373–85
    [Google Scholar]
  104. Sheth SN, Angert AL. 2018. Demographic compensation does not rescue populations at a trailing range edge. PNAS 115:2413–18
    [Google Scholar]
  105. Singhal S, Huang H, Grundler MR, Marchán-Rivadeneira MR, Holmes I et al. 2018. Does population structure predict the rate of speciation? A comparative test across Australia's most diverse vertebrate radiation. Am. Nat. 192:432–47
    [Google Scholar]
  106. Smits PD. 2015. Expected time-invariant effects of biological traits on mammal species duration. PNAS 112:13015–20
    [Google Scholar]
  107. Stanley SM. 1986. Population size, extinction, and speciation: the fission effect in Neogene Bivalvia. Paleobiology 12:89–110
    [Google Scholar]
  108. Tingley MW, Monahan WB, Beissinger SR, Moritz C 2009. Birds track their Grinnellian niche through a century of climate change. PNAS 106:19637–43
    [Google Scholar]
  109. Turelli M, Barton NH, Coyne JA 2001. Theory and speciation. Trends Ecol. Evol. 16:330–43
    [Google Scholar]
  110. Valente LM, Phillimore AB, Etienne RS 2015. Equilibrium and non-equilibrium dynamics simultaneously operate in the Galápagos Islands. Ecol. Lett. 18:844–52
    [Google Scholar]
  111. van der Valk T, Díez-del Molino D, Marques-Bonet T, Guschanski K, Dalén L 2019. Historical genomes reveal the genomic consequences of recent population decline in eastern gorillas. Curr. Biol. 29:165–70
    [Google Scholar]
  112. Villanea FA, Schraiber JG. 2019. Multiple episodes of interbreeding between Neanderthal and modern humans. Nat. Ecol. Evol. 3:39
    [Google Scholar]
  113. Wang S, Chen A, Fang J, Pacala SW 2013. Speciation rates decline through time in individual-based models of speciation and extinction. Am. Nat. 182:E83–93
    [Google Scholar]
  114. Weeks BC, Claramunt S. 2014. Dispersal has inhibited avian diversification in Australasian archipelagos. Proc. R. Soc. B 281:20141257
    [Google Scholar]
  115. Weir JT, Schluter D. 2007. The latitudinal gradient in recent speciation and extinction rates of birds and mammals. Science 315:1574–76
    [Google Scholar]
  116. Wright S. 1931. Evolution in Mendelian populations. Genetics 16:97
    [Google Scholar]
  117. Wright S. 1932. The roles of mutation, inbreeding, crossbreeding, and selection in evolution. Proc. Sixth Int. Congr. Genet. 1:356–66
    [Google Scholar]
  118. Wright S. 1940. Breeding structure of populations in relation to speciation. Am. Nat. 74:232–48
    [Google Scholar]
  119. Wright S. 1943. Isolation by distance. Genetics 28:114
    [Google Scholar]
  120. Wu CI. 2001. The genic view of the process of speciation. J. Evol. Biol. 14:851–65
    [Google Scholar]
/content/journals/10.1146/annurev-ecolsys-110218-024701
Loading
/content/journals/10.1146/annurev-ecolsys-110218-024701
Loading

Data & Media loading...

Supplementary Data

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error