Identifying the transition between single and multiple mating of queens in fungus-growing ants

Palle Villesen, Takahiro Murakami, Ted R. Schultz, Jacobus J. Boomsma

Research output: Contribution to journalArticle

93 Citations (Scopus)

Abstract

Obligate mating of females (queens) with multiple males has evolved only rarely in social Hymenoptera (ants, social bees, social wasps) and for reasons that are fundamentally different from those underlying multiple mating in other animals. The monophyletic tribe of ('attine') fungus-growing ants is known to include evolutionarily derived genera with obligate multiple mating (the Acromyrmex and Atta leafcutter ants) as well as phylogenetically basal genera with exclusively single mating (e.g. Apterostigma, Cyphomyrmex, Myrmicocrypta). All attine genera share the unique characteristic of obligate dependence on symbiotic fungus gardens for food, but the sophistication of this symbiosis differs considerably across genera. The lower attine genera generally have small, short-lived colonies and relatively non-specialized fungal symbionts (capable of living independently of their ant hosts), whereas the four evolutionarily derived higher attine genera have highly specialized, long-term clonal symbionts. In this paper, we investigate whether the transition from single to multiple mating occurred relatively recently in the evolution of the attine ants, in conjunction with the novel herbivorous 'leafcutter' niche acquired by the common ancestor of Acromyrmex and Atta, or earlier, at the transition to rearing specialized long-term clonal fungi in the common ancestor of the larger group of higher attines that also includes the genera Trachymyrmex and Sericomyrmex. We use DNA microsatellite analysis to provide unambiguous evidence for a single, late and abrupt evolutionary transition from exclusively single to obligatory multiple mating. This transition is historically correlated with other evolutionary innovations, including the extensive use of fresh vegetation as substrate for the fungus garden, a massive increase in mature colony size and morphological differentiation of the worker caste.

Original languageEnglish
Pages (from-to)1541-1548
Number of pages8
JournalProceedings of the Royal Society B: Biological Sciences
Volume269
Issue number1500
DOIs
Publication statusPublished - Aug 7 2002
Externally publishedYes

Fingerprint

multiple mating
Ants
Fungi
queen insects
ant
Formicidae
fungus
fungi
Acromyrmex
Atta
common ancestry
symbiont
symbionts
garden
Sericomyrmex
Myrmicocrypta
Apterostigma
Cyphomyrmex
Trachymyrmex
ancestry

All Science Journal Classification (ASJC) codes

  • Agricultural and Biological Sciences(all)
  • Agricultural and Biological Sciences (miscellaneous)

Cite this

Identifying the transition between single and multiple mating of queens in fungus-growing ants. / Villesen, Palle; Murakami, Takahiro; Schultz, Ted R.; Boomsma, Jacobus J.

In: Proceedings of the Royal Society B: Biological Sciences, Vol. 269, No. 1500, 07.08.2002, p. 1541-1548.

Research output: Contribution to journalArticle

@article{3407bb16ecf14a2c994721b1ffabd89a,
title = "Identifying the transition between single and multiple mating of queens in fungus-growing ants",
abstract = "Obligate mating of females (queens) with multiple males has evolved only rarely in social Hymenoptera (ants, social bees, social wasps) and for reasons that are fundamentally different from those underlying multiple mating in other animals. The monophyletic tribe of ('attine') fungus-growing ants is known to include evolutionarily derived genera with obligate multiple mating (the Acromyrmex and Atta leafcutter ants) as well as phylogenetically basal genera with exclusively single mating (e.g. Apterostigma, Cyphomyrmex, Myrmicocrypta). All attine genera share the unique characteristic of obligate dependence on symbiotic fungus gardens for food, but the sophistication of this symbiosis differs considerably across genera. The lower attine genera generally have small, short-lived colonies and relatively non-specialized fungal symbionts (capable of living independently of their ant hosts), whereas the four evolutionarily derived higher attine genera have highly specialized, long-term clonal symbionts. In this paper, we investigate whether the transition from single to multiple mating occurred relatively recently in the evolution of the attine ants, in conjunction with the novel herbivorous 'leafcutter' niche acquired by the common ancestor of Acromyrmex and Atta, or earlier, at the transition to rearing specialized long-term clonal fungi in the common ancestor of the larger group of higher attines that also includes the genera Trachymyrmex and Sericomyrmex. We use DNA microsatellite analysis to provide unambiguous evidence for a single, late and abrupt evolutionary transition from exclusively single to obligatory multiple mating. This transition is historically correlated with other evolutionary innovations, including the extensive use of fresh vegetation as substrate for the fungus garden, a massive increase in mature colony size and morphological differentiation of the worker caste.",
author = "Palle Villesen and Takahiro Murakami and Schultz, {Ted R.} and Boomsma, {Jacobus J.}",
year = "2002",
month = "8",
day = "7",
doi = "10.1098/rspb.2002.2044",
language = "English",
volume = "269",
pages = "1541--1548",
journal = "Proceedings of the Royal Society B: Biological Sciences",
issn = "0962-8452",
publisher = "Royal Society of London",
number = "1500",

}

TY - JOUR

T1 - Identifying the transition between single and multiple mating of queens in fungus-growing ants

AU - Villesen, Palle

AU - Murakami, Takahiro

AU - Schultz, Ted R.

AU - Boomsma, Jacobus J.

PY - 2002/8/7

Y1 - 2002/8/7

N2 - Obligate mating of females (queens) with multiple males has evolved only rarely in social Hymenoptera (ants, social bees, social wasps) and for reasons that are fundamentally different from those underlying multiple mating in other animals. The monophyletic tribe of ('attine') fungus-growing ants is known to include evolutionarily derived genera with obligate multiple mating (the Acromyrmex and Atta leafcutter ants) as well as phylogenetically basal genera with exclusively single mating (e.g. Apterostigma, Cyphomyrmex, Myrmicocrypta). All attine genera share the unique characteristic of obligate dependence on symbiotic fungus gardens for food, but the sophistication of this symbiosis differs considerably across genera. The lower attine genera generally have small, short-lived colonies and relatively non-specialized fungal symbionts (capable of living independently of their ant hosts), whereas the four evolutionarily derived higher attine genera have highly specialized, long-term clonal symbionts. In this paper, we investigate whether the transition from single to multiple mating occurred relatively recently in the evolution of the attine ants, in conjunction with the novel herbivorous 'leafcutter' niche acquired by the common ancestor of Acromyrmex and Atta, or earlier, at the transition to rearing specialized long-term clonal fungi in the common ancestor of the larger group of higher attines that also includes the genera Trachymyrmex and Sericomyrmex. We use DNA microsatellite analysis to provide unambiguous evidence for a single, late and abrupt evolutionary transition from exclusively single to obligatory multiple mating. This transition is historically correlated with other evolutionary innovations, including the extensive use of fresh vegetation as substrate for the fungus garden, a massive increase in mature colony size and morphological differentiation of the worker caste.

AB - Obligate mating of females (queens) with multiple males has evolved only rarely in social Hymenoptera (ants, social bees, social wasps) and for reasons that are fundamentally different from those underlying multiple mating in other animals. The monophyletic tribe of ('attine') fungus-growing ants is known to include evolutionarily derived genera with obligate multiple mating (the Acromyrmex and Atta leafcutter ants) as well as phylogenetically basal genera with exclusively single mating (e.g. Apterostigma, Cyphomyrmex, Myrmicocrypta). All attine genera share the unique characteristic of obligate dependence on symbiotic fungus gardens for food, but the sophistication of this symbiosis differs considerably across genera. The lower attine genera generally have small, short-lived colonies and relatively non-specialized fungal symbionts (capable of living independently of their ant hosts), whereas the four evolutionarily derived higher attine genera have highly specialized, long-term clonal symbionts. In this paper, we investigate whether the transition from single to multiple mating occurred relatively recently in the evolution of the attine ants, in conjunction with the novel herbivorous 'leafcutter' niche acquired by the common ancestor of Acromyrmex and Atta, or earlier, at the transition to rearing specialized long-term clonal fungi in the common ancestor of the larger group of higher attines that also includes the genera Trachymyrmex and Sericomyrmex. We use DNA microsatellite analysis to provide unambiguous evidence for a single, late and abrupt evolutionary transition from exclusively single to obligatory multiple mating. This transition is historically correlated with other evolutionary innovations, including the extensive use of fresh vegetation as substrate for the fungus garden, a massive increase in mature colony size and morphological differentiation of the worker caste.

UR - http://www.scopus.com/inward/record.url?scp=0037036628&partnerID=8YFLogxK

UR - http://www.scopus.com/inward/citedby.url?scp=0037036628&partnerID=8YFLogxK

U2 - 10.1098/rspb.2002.2044

DO - 10.1098/rspb.2002.2044

M3 - Article

C2 - 12184823

AN - SCOPUS:0037036628

VL - 269

SP - 1541

EP - 1548

JO - Proceedings of the Royal Society B: Biological Sciences

JF - Proceedings of the Royal Society B: Biological Sciences

SN - 0962-8452

IS - 1500

ER -