Modeling the maintenance of a dependent lineage system: The influence of positive frequency-dependent selection on sex ratio

Kirk E. Anderson, Chris R. Smith, Timothy A. Linksvayer, Brendon M. Mott, Juergen Gadau, Jennifer Fewell

    Research output: Contribution to journalArticle

    11 Citations (Scopus)

    Abstract

    In insect societies, worker versus queen development (reproductive caste) is typically governed by environmental factors, but some Pogonomyrmex seed-harvester ants exhibit strict genetic caste determination, resulting in an obligate mutualism between two reproductively isolated lineages. Queens mate randomly with multiple males from each lineage and intralineage crosses produce new queens, whereas interlineage crosses produce workers. Early colony survival is negatively frequency dependent; when lineage frequencies are unequal, queens from the rarer lineage benefit because they acquire more interlineage sperm, and produce more workers. Here we examine theoretically and empirically the effect of relative lineage frequency on sex ratio. We predict that the ratio of inter- to intralineage sperm acquired by queens of each lineage will affect the sex ratio produced at colony maturity. Consistent with model predictions, we found that gyne production in mature colonies was positively frequency dependent, increasing significantly with increasing lineage frequency across 15 populations. Unequal lineage frequencies are common and likely maintained by a complex interplay between an ecological advantage specific to one lineage, and opposing frequency-dependent selection pressures experienced throughout the colonies life-cycle; rare lineage colonies benefit during early colony growth, and common lineage colonies benefit at reproductive maturity.

    Original languageEnglish (US)
    Pages (from-to)2142-2152
    Number of pages11
    JournalEvolution
    Volume63
    Issue number8
    DOIs
    StatePublished - Aug 2009

    Fingerprint

    Sex Ratio
    Social Class
    sex ratio
    Spermatozoa
    Maintenance
    queen insects
    Symbiosis
    Ants
    Life Cycle Stages
    modeling
    Insects
    Seeds
    caste
    Pressure
    sperm
    Growth
    Population
    Pogonomyrmex
    spermatozoa
    caste determination

    Keywords

    • Dependent lineage
    • Frequency-dependent selection
    • Inclusive fitness
    • Obligate mutualism
    • Polyphenism
    • Sex allocation
    • Symmetrical social hybridogenesis

    ASJC Scopus subject areas

    • Agricultural and Biological Sciences(all)
    • Ecology, Evolution, Behavior and Systematics
    • Genetics

    Cite this

    Modeling the maintenance of a dependent lineage system : The influence of positive frequency-dependent selection on sex ratio. / Anderson, Kirk E.; Smith, Chris R.; Linksvayer, Timothy A.; Mott, Brendon M.; Gadau, Juergen; Fewell, Jennifer.

    In: Evolution, Vol. 63, No. 8, 08.2009, p. 2142-2152.

    Research output: Contribution to journalArticle

    Anderson, Kirk E. ; Smith, Chris R. ; Linksvayer, Timothy A. ; Mott, Brendon M. ; Gadau, Juergen ; Fewell, Jennifer. / Modeling the maintenance of a dependent lineage system : The influence of positive frequency-dependent selection on sex ratio. In: Evolution. 2009 ; Vol. 63, No. 8. pp. 2142-2152.
    @article{a850d0744e1547f498ad80a4a0c9ca6b,
    title = "Modeling the maintenance of a dependent lineage system: The influence of positive frequency-dependent selection on sex ratio",
    abstract = "In insect societies, worker versus queen development (reproductive caste) is typically governed by environmental factors, but some Pogonomyrmex seed-harvester ants exhibit strict genetic caste determination, resulting in an obligate mutualism between two reproductively isolated lineages. Queens mate randomly with multiple males from each lineage and intralineage crosses produce new queens, whereas interlineage crosses produce workers. Early colony survival is negatively frequency dependent; when lineage frequencies are unequal, queens from the rarer lineage benefit because they acquire more interlineage sperm, and produce more workers. Here we examine theoretically and empirically the effect of relative lineage frequency on sex ratio. We predict that the ratio of inter- to intralineage sperm acquired by queens of each lineage will affect the sex ratio produced at colony maturity. Consistent with model predictions, we found that gyne production in mature colonies was positively frequency dependent, increasing significantly with increasing lineage frequency across 15 populations. Unequal lineage frequencies are common and likely maintained by a complex interplay between an ecological advantage specific to one lineage, and opposing frequency-dependent selection pressures experienced throughout the colonies life-cycle; rare lineage colonies benefit during early colony growth, and common lineage colonies benefit at reproductive maturity.",
    keywords = "Dependent lineage, Frequency-dependent selection, Inclusive fitness, Obligate mutualism, Polyphenism, Sex allocation, Symmetrical social hybridogenesis",
    author = "Anderson, {Kirk E.} and Smith, {Chris R.} and Linksvayer, {Timothy A.} and Mott, {Brendon M.} and Juergen Gadau and Jennifer Fewell",
    year = "2009",
    month = "8",
    doi = "10.1111/j.1558-5646.2009.00696.x",
    language = "English (US)",
    volume = "63",
    pages = "2142--2152",
    journal = "Evolution; international journal of organic evolution",
    issn = "0014-3820",
    publisher = "Society for the Study of Evolution",
    number = "8",

    }

    TY - JOUR

    T1 - Modeling the maintenance of a dependent lineage system

    T2 - The influence of positive frequency-dependent selection on sex ratio

    AU - Anderson, Kirk E.

    AU - Smith, Chris R.

    AU - Linksvayer, Timothy A.

    AU - Mott, Brendon M.

    AU - Gadau, Juergen

    AU - Fewell, Jennifer

    PY - 2009/8

    Y1 - 2009/8

    N2 - In insect societies, worker versus queen development (reproductive caste) is typically governed by environmental factors, but some Pogonomyrmex seed-harvester ants exhibit strict genetic caste determination, resulting in an obligate mutualism between two reproductively isolated lineages. Queens mate randomly with multiple males from each lineage and intralineage crosses produce new queens, whereas interlineage crosses produce workers. Early colony survival is negatively frequency dependent; when lineage frequencies are unequal, queens from the rarer lineage benefit because they acquire more interlineage sperm, and produce more workers. Here we examine theoretically and empirically the effect of relative lineage frequency on sex ratio. We predict that the ratio of inter- to intralineage sperm acquired by queens of each lineage will affect the sex ratio produced at colony maturity. Consistent with model predictions, we found that gyne production in mature colonies was positively frequency dependent, increasing significantly with increasing lineage frequency across 15 populations. Unequal lineage frequencies are common and likely maintained by a complex interplay between an ecological advantage specific to one lineage, and opposing frequency-dependent selection pressures experienced throughout the colonies life-cycle; rare lineage colonies benefit during early colony growth, and common lineage colonies benefit at reproductive maturity.

    AB - In insect societies, worker versus queen development (reproductive caste) is typically governed by environmental factors, but some Pogonomyrmex seed-harvester ants exhibit strict genetic caste determination, resulting in an obligate mutualism between two reproductively isolated lineages. Queens mate randomly with multiple males from each lineage and intralineage crosses produce new queens, whereas interlineage crosses produce workers. Early colony survival is negatively frequency dependent; when lineage frequencies are unequal, queens from the rarer lineage benefit because they acquire more interlineage sperm, and produce more workers. Here we examine theoretically and empirically the effect of relative lineage frequency on sex ratio. We predict that the ratio of inter- to intralineage sperm acquired by queens of each lineage will affect the sex ratio produced at colony maturity. Consistent with model predictions, we found that gyne production in mature colonies was positively frequency dependent, increasing significantly with increasing lineage frequency across 15 populations. Unequal lineage frequencies are common and likely maintained by a complex interplay between an ecological advantage specific to one lineage, and opposing frequency-dependent selection pressures experienced throughout the colonies life-cycle; rare lineage colonies benefit during early colony growth, and common lineage colonies benefit at reproductive maturity.

    KW - Dependent lineage

    KW - Frequency-dependent selection

    KW - Inclusive fitness

    KW - Obligate mutualism

    KW - Polyphenism

    KW - Sex allocation

    KW - Symmetrical social hybridogenesis

    UR - http://www.scopus.com/inward/record.url?scp=68149107580&partnerID=8YFLogxK

    UR - http://www.scopus.com/inward/citedby.url?scp=68149107580&partnerID=8YFLogxK

    U2 - 10.1111/j.1558-5646.2009.00696.x

    DO - 10.1111/j.1558-5646.2009.00696.x

    M3 - Article

    VL - 63

    SP - 2142

    EP - 2152

    JO - Evolution; international journal of organic evolution

    JF - Evolution; international journal of organic evolution

    SN - 0014-3820

    IS - 8

    ER -