hippocampal representations are highly task-dependent, plastic, and memory-dependent (30–32).
Additionally, this task created a high level of social
interactions between the two bats: When the bats
were together at the start ball, they often approached and touched each other and emitted
many social vocalizations (fig. S8), and this intensely social situation may have contributed to
the representation of the conspecific.
There is an apparent similarity between the
social place-cells, which encode the position of
the other, and “mirror neurons” in monkeys,
which encode the actions of the other (33). One
difference, however, is that noncongruent social
place-cells (Fig. 1C, cells 358 and 254) are still
useful functionally because they encode meaningful information about the position of the other,
whereas it is less clear how noncongruent mirror
neurons in monkeys might be useful for the
proposed functions of mirror neurons. Thus, social
place-cells are conceptually different from mirror
neurons, although both might possibly share a similar functional principle, whereby the same neuronal circuit can be used for self-representation as
well as for representing conspecifics.
Last, we speculate that social place-cells may
play a role in a wide range of social behaviors in
many species—from group navigation and coordinated hunting to observational learning,
social hierarchy, and courtship—and may be relevant also for the representation of nonconspecific
animals—for example, for spatial encoding of predators and prey. These results open many questions
for future studies: How are multiple animals represented in the brain? Is there a different representation for socially dominant versus subordinate
animals, and for males versus females? These and
many other questions await investigation in order to elucidate the neural basis of social-spatial
REFERENCES AND NOTES
1. J. O’Keefe, L. Nadel, The Hippocampus as a Cognitive Map
(Oxford Univ. Press, 1978).
2. M. A. Wilson, B. L. McNaughton, Science 261, 1055–1058
3. N. Ulanovsky, C. F. Moss, Nat. Neurosci. 10, 224–233 (2007).
4. T. Hafting, M. Fyhn, S. Molden, M.-B. Moser, E. I. Moser, Nature
436, 801–806 (2005).
5. C. Barry, R. Hayman, N. Burgess, K. J. Jeffery, Nat. Neurosci.
10, 682–684 (2007).
6. M. M. Yartsev, M. P. Witter, N. Ulanovsky, Nature 479, 103–107
7. J. S. Taube, R. U. Muller, J. B. Ranck Jr., J. Neurosci. 10,
8. A. Peyrache, M. M. Lacroix, P. C. Petersen, G. Buzsáki,
Nat. Neurosci. 18, 569–575 (2015).
9. A. Finkelstein et al., Nature 517, 159–164 (2015).
10. T. Solstad, C. N. Boccara, E. Kropff, M.-B. Moser, E. I. Moser,
Science 322, 1865–1868 (2008).
11. F. Savelli, D. Yoganarasimha, J. J. Knierim, Hippocampus 18,
12. C. Lever, S. Burton, A. Jeewajee, J. O’Keefe, N. Burgess,
J. Neurosci. 29, 9771–9777 (2009).
13. G. Neuweiler, The Biology of Bats (Oxford Univ. Press, 2000).
14. Materials and methods are available as supplementary
15. M. M. Yartsev, N. Ulanovsky, Science 340, 367–372 (2013).
16. B. E. Pfeiffer, D. J. Foster, Science 349, 180–183 (2015).
17. J. Ferbinteanu, M. L. Shapiro, Neuron 40, 1227–1239
18. T. J. Davidson, F. Kloosterman, M. A. Wilson, Neuron 63,
19. A. Sarel, A. Finkelstein, L. Las, N. Ulanovsky, Science 355,
20. S. A. Ho et al., Neuroscience 157, 254–270 (2008).
21. E. J. Henriksen et al., Neuron 68, 127– 137 (2010).
22. A. Tsao, M.-B. Moser, E. I. Moser, Curr. Biol. 23, 399–405 (2013).
23. J. J. Knierim, J. P. Neunuebel, S. S. Deshmukh, Philos. Trans. R.
Soc. Lond. B Biol. Sci. 369, 20130369 (2013).
24. F. L. Hitti, S. A. Siegelbaum, Nature 508, 88–92 (2014).
25. S. M. Dudek, G. M. Alexander, S. Farris, Nat. Rev. Neurosci. 17,
26. T. Okuyama, T. Kitamura, D. S. Roy, S. Itohara, S. Tonegawa,
Science 353, 1536–1541 (2016).
27. L. Zynyuk, J. Huxter, R. U. Muller, S. E. Fox, Hippocampus 22,
28. M. von Heimendahl, R. P. Rao, M. Brecht, J. Neurosci. 32,
29. X. Mou, D. Ji, eLife 5, e18022 (2016).
30. E. J. Markus et al., J. Neurosci. 15, 7079–7094 (1995).
31. M. A. Moita, S. Rosis, Y. Zhou, J. E. LeDoux, H. T. Blair, Neuron
37, 485–497 (2003).
32. H. Eichenbaum, N. J. Cohen, Neuron 83, 764–770 (2014).
33. G. Rizzolatti, C. Sinigaglia, Nat. Rev. Neurosci. 17, 757–765 (2016).
We thank K. Haroush, S. Romani, O. Forkosh, A. Rubin, M. Geva-Sagiv,
A. Finkelstein, T. Eliav, G. Ginosar, A. Sarel, and D. Blum for
comments on the manuscript; S. Kaufman, O. Gobi, and S. Futerman
for bat training; A. Tuval for veterinary support; C. Ra’anan and
R. Eilam for histology; B. Pasmantirer and G. Ankaoua for
mechanical designs; and G. Brodsky for graphics. This study was
supported by research grants to N.U. from the European
Research Council (ERC-CoG–NATURAL_BAT_NAV), Israel Science
Foundation (ISF 1319/13), and Minerva Foundation. The data are
archived on the Weizmann Institute of Science servers and will be
made available on request.
Materials and Methods
Figs. S1 to S8
Movies S1 and S2
11 July 2017; accepted 7 December 2017
Rapid hybrid speciation in
Sangeet Lamichhaney,1 Fan Han,1 Matthew T. Webster,1 Leif Andersson,1,2,3†
B. Rosemary Grant,4 Peter R. Grant4
Homoploid hybrid speciation in animals has been inferred frequently from patterns of
variation, but few examples have withstood critical scrutiny. Here we report a directly
documented example, from its origin to reproductive isolation. An immigrant Darwin’s finch to
Daphne Major in the Galápagos archipelago initiated a new genetic lineage by breeding with
a resident finch (Geospiza fortis). Genome sequencing of the immigrant identified it as a
G. conirostris male that originated on Española >100 kilometers from Daphne Major. From the
second generation onward, the lineage bred endogamously and, despite intense inbreeding,
was ecologically successful and showed transgressive segregation of bill morphology.
This example shows that reproductive isolation, which typically develops over hundreds of
generations, can be established in only three.
Interbreeding of two species may result in the formation of a new species, reproductively iso- lated from the parental species (1). Hybrid speciation without chromosomal doubling, that is, homoploid hybrid speciation, is rare
(1–4). Possible examples have been reported in
plants (4), butterflies (5), flies (6), fish (7), mammals
(8), and birds (9). However, only one of these,
involving Heliconius butterflies (5), and three ad-
ditional examples, involving Helianthus sun-
flowers (3, 10), meet stringent criteria that have
been proposed for recognizing that hybridization
was the cause of speciation (2). Here we report
the results of a combined ecological and genomic
study of Darwin’s finches that documents hybrid
speciation in the wild from its inception to the
development of reproductive isolation.
An immature male finch immigrated to the
small Galápagos Island of Daphne Major (0.34 km2)
in 1981 (11–13). It resembled the medium ground
finch Geospiza fortis, but was 70% larger and
sang a distinctive song. Assignment tests with mi-crosatellite markers from finches on neighboring
islands indicated that it was possibly a G. fortis ×
G. scandens hybrid originating on the adjacent
large island of Santa Cruz, 8 km from Daphne (11).
We followed the survival and breeding of this individual and its descendants for six generations
over the next 31 years.
The immigrant (generation 0) bred with a
G. fortis female and one of its F1 offspring bred
with another G. fortis female, but all other matings
occurred within this lineage, endogamously; therefore, from generation 2 onward, the lineage behaved as an independent species relative to other
birds on the island (Fig. 1). Generations 4 to 6
were derived from a single brother-sister mating
1Department of Medical Biochemistry and Microbiology,
Uppsala University, Uppsala, Sweden. 2Department of Animal
Breeding and Genetics, Swedish University of Agricultural
Sciences, Uppsala, Sweden. 3Department of Veterinary
Integrative Biosciences, Texas A&M University, College
Station, TX, USA. 4Department of Ecology and Evolutionary
Biology, Princeton University, Princeton, NJ, USA.
*Present address: Department of Organismic and Evolutionary
Biology and Museum of Comparative Zoology, Harvard University,
Cambridge, MA, USA.
†Corresponding author. Email: firstname.lastname@example.org