Multiple Origins of Eusociality Among Sponge-Dwelling Shrimps (Synalpheus)

Duffy, J. Emmett; Morrison, Cheryl L.; Rubén, R; íos,

doi:10.1111/j.0014-3820.2000.tb00053.x

Cited by 107 publications

(49 citation statements)

References 67 publications

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“…Although eusociality has evolved repeatedly in Synalpheus (Duffy et al 2000;Morrison et al 2004;Didderen et al 2006), our phylogenetically controlled tests using new data for both development mode and social organization showed that eusociality was almost perfectly correlated with direct development, in which eggs hatch as crawling juveniles (figure 2). This association held regardless of whether the apparently variable species S. idios was coded as having swimming larvae (Maddison's CCT, p ¼ 0.005 -0.006 for the five trees) or crawling larvae (p ¼ 0.014 -0.016 for the five trees).…”

Section: Resultsmentioning

confidence: 86%

“…The calculation, assumptions and rationale for using the E index for Synalpheus have been described previously (Duffy et al 2000). Briefly, the E index accounts for both reproductive skew and colony size, both of which vary considerably among Synalpheus species, and the index can be calculated from data collected over short time spans such as the point estimates available from our collections.…”

Section: (D) Quantifying Socialitymentioning

confidence: 99%

“…Natural history suggests that ecological constraints are a key factor in the evolution of shrimp sociality: host sponges provide both habitat and food, nearly all hosts are occupied in the field (Duffy 1996b;Duffy et al 2000), and shrimp defend them fiercely against intruders (Duffy 1996a;Duffy et al 2002;Tó th & Duffy 2005), indicating that habitat is valuable and in short supply. These observations appear consistent with both the habitat saturation hypothesis (Selander 1964;Emlen 1982) and the fortress defence model (Crespi 1994;Queller & Strassmann 1998), but they provide only indirect evidence in support of ecological drivers of social evolution.…”

Section: Introductionmentioning

confidence: 99%

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Kin structure, ecology and the evolution of social organization in shrimp: a comparative analysis

2009

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Eusocial societies present a Darwinian paradox, yet they have evolved independently in insects, mole-rats and symbiotic shrimp. Historically, eusociality has been thought to arise as a response to ecological challenges, mediated by kin selection, but the role of kin selection has recently been questioned. Here we use phylogenetically independent contrasts to test the association of eusociality with ecological performance and genetic structure (via life history) among 20 species of sponge-dwelling shrimp (Synalpheus) in Belize. Consistent with hypotheses that cooperative groups enjoy an advantage in challenging habitats, we show that eusocial species are more abundant, occupy more sponges and have broader host ranges than nonsocial sister species, and that these patterns are robust to correction for the generally smaller body sizes of eusocial species. In contrast, body size explains less or no variation after accounting for sociality. Despite strong ecological pressures on most sponge-dwellers, however, eusociality arose only in species with non-dispersing larvae, which form family groups subject to kin selection. Thus, superior ability to hold valuable resources may favour eusociality in shrimp but close genetic relatedness is nevertheless key to its origin, as in other eusocial animals.

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Section: Resultsmentioning

confidence: 86%

Section: (D) Quantifying Socialitymentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Kin structure, ecology and the evolution of social organization in shrimp: a comparative analysis

2009

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“…(d) Social structure Social structure was estimated using a variation of the eusociality index [38], calculated as E ¼ 1 2 (2 Â Q)/N, where N is colony size and Q is the number of reproductive females (sensu [22,23]). The eusociality index (E) incorporates both a colony's size and its reproductive skew making the simplifying assumption that all breeding individuals contribute equally to offspring production.…”

Section: (C) Reproductive Maturity and Sex Ratiosmentioning

confidence: 99%

Reproductive skew drives patterns of sexual dimorphism in sponge-dwelling snapping shrimps

2015

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Sexual dimorphism is typically a result of strong sexual selection on male traits used in male-male competition and subsequent female choice. However, in social species where reproduction is monopolized by one or a few individuals in a group, selection on secondary sexual characteristics may be strong in both sexes. Indeed, sexual dimorphism is reduced in many cooperatively breeding vertebrates and eusocial insects with totipotent workers, presumably because of increased selection on female traits. Here, we examined the relationship between sexual dimorphism and sociality in eight species of Synalpheus snapping shrimps that vary in social structure and degree of reproductive skew. In species where reproduction was shared more equitably, most members of both sexes were physiologically capable of breeding. However, in species where reproduction was monopolized by a single individual, a large proportion of females-but not males-were reproductively inactive, suggesting stronger reproductive suppression and conflict among females. Moreover, as skew increased across species, proportional size of the major chela-the primary antagonistic weapon in snapping shrimps-increased among females and sexual dimorphism in major chela size declined. Thus, as reproductive skew increases among Synalpheus, female-female competition over reproduction appears to increase, resulting in decreased sexual dimorphism in weapon size.

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“…The idea that co-operating groups can attend and defend resources more efficiently than individuals or less organised groups, and that eusociality may evolve by intense interactive competition for limited resources has existed for some time (Lin and Michener 1972;Alexander 1974;Evans 1977;Emlen 1991;Duffy et al 2000). The hypothesis was formalised by Witting (1997Witting ( , 2002b, who showed that if the level of interactive competition is sufficiently large, as is expected if the body mass is upward evolutionarily constrained relative to the energetic state of the organism (Section IV.2), then selection by density-dependent competitive interactions will select for large interacting units with the evolutionary optimum to the composition of individuals in the unit being a single female, a single male and a large number offspring workers that are sexually produced by the male and female (Witting 2002b).…”

Section: Eusocial Coloniesmentioning

confidence: 99%

Inevitable evolution: back toThe Originand beyond the 20th Century paradigm of contingent evolution by historical natural selection

Witting¹

2008

Biological Reviews

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Since neo-Darwinism arose from the work of Darwin and Mendel evolution by natural selection has been seen as contingent and historical being defined by an a posteriori selection process with no a priori laws that explain why evolution on Earth has taken the direction of the major evolutionary trends and transitions instead of any other direction. Recently, however, major life-history trends and transitions have been explained as inevitable because of a deterministic selection that unfolds from the energetic state of the organism and the density-dependent competitive interactions that arise from self-replication in limited environments. I describe differences and similarities between the historical and deterministic selection processes, illustrate concepts using life-history models on large body masses and limited reproductive rates, review life-history evolution with a wider focus on major evolutionary transitions, and propose that biotic evolution is driven by a universal natural selection where the long-term evolution of fitness-related traits is determined mainly by deterministic selection, while contingency is important predominately for neutral traits. Given suitable environmental conditions, it is shown that selection by energetic state and densitydependent competitive interactions unfolds to higher level selection for life-history transitions from simple asexually reproducing self-replicators to large bodied organisms with senescence and sexual reproduction between males and females, and in some cases, to the fully evolved eusocial colony with thousands of offspring workers. This defines an evolutionary arrow of time for open thermodynamic systems with a constant inflow of energy, predicting similar routes for long-term evolution on similar planets.

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Multiple Origins of Eusociality Among Sponge-Dwelling Shrimps (Synalpheus)

Cited by 107 publications

References 67 publications

Kin structure, ecology and the evolution of social organization in shrimp: a comparative analysis

Kin structure, ecology and the evolution of social organization in shrimp: a comparative analysis

Reproductive skew drives patterns of sexual dimorphism in sponge-dwelling snapping shrimps

Inevitable evolution: back toThe Originand beyond the 20th Century paradigm of contingent evolution by historical natural selection

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