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, 99 (1), 286-90

Evolution of Sociality in a Primitively Eusocial Lineage of Bees

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Evolution of Sociality in a Primitively Eusocial Lineage of Bees

Bryan N Danforth. Proc Natl Acad Sci U S A.

Abstract

Eusociality is a major evolutionary innovation involving alterations in life history, morphology, and behavior. Advanced eusocial insects, such as ants, termites, and corbiculate bees, cannot provide insights into the earliest stages of eusocial evolution because eusociality in these taxa evolved long ago (in the Cretaceous) and close solitary relatives are no longer extant. In contrast, primitively eusocial insects, such as halictid bees, provide insights into the early stages of eusocial evolution because eusociality has arisen recently and repeatedly. By mapping social behavior onto well-corroborated phylogenies, I show that eusociality has arisen only three times within halictid bees (contrary to earlier estimates of six or more origins). Reversals from eusocial to solitary behavior have occurred as many as 12 times, indicating that social reversals are common in the earliest stages of eusocial evolution. Important attributes of social complexity (e.g., colony size, queen/worker dimorphism) show no obvious association with phylogeny, and some reversals to solitary nesting are related to host-plant switches (from polylecty to oligolecty). These results provide a glimpse of social evolution in its earliest stages and provide insights into the early evolution of advanced eusocial organisms.

Figures

Figure 1
Figure 1
Phylogeny of the halictid subfamilies, tribes, and genera. Strict consensus of six trees based on equal weights parsimony analysis of the entire data set (spanning positions 145-1271 in the coding region of the Apis mellifera F2 copy). The data set includes three exons and two introns. Two regions within the introns were excluded because they could not be aligned unambiguously. Gaps coded as a fifth state or according to the methods described in ref. yielded the same six trees. Bootstrap values above the nodes indicate bootstrap support based on the exons + introns data set. Bootstrap values below the nodes indicate support based on an analysis of exons only. For the exons + introns analysis the data set included 1,541 total aligned sites (619 parsimony-informative sites), the trees were 3,388 steps in length, and the consistency index (excluding uninformative sites) was 0.3831. For the exons-only analysis there were 1,127 aligned sites (327 parsimony-informative sites), the trees were 1,648 steps in length, and the consistency index (excluding uninformative sites) was 0.3195. The tree was rooted by using a colletid bee (Leioproctus sp.). Maximum-likelihood analyses using the K2P model with rate heterogeneity accounted for by site-specific rates yielded the same overall tree topology irrespective of whether exons or exons + introns were analyzed. Clades inferred to have a eusocial common ancestor (see text) are shown in blue. Cleptoparasitic taxa (Sphecodes) are shown in red. Three origins of eusociality (indicated by blue bars) are indicated on the cladogram.
Figure 2
Figure 2
Phylogeny of the species and subgenera of Halictus based on elongation factor-1α. Details of the phylogenetic analysis are presented in ref. . Social behavior was mapped onto the tree by using macclade version 3.07 (27). Socially polymorphic taxa are those in which solitary as well as eusocial populations are known to occur within the same species. Equivocal branches are those in which ancestral character states could not be unambiguously inferred given the tree topology and available behavioral data.
Figure 3
Figure 3
Phylogeny of the eusocial clade of Lasioglossum. One of six trees based on equal weights parsimony analysis of the combined cytochrome oxidase I (COI) (24) and elongation factor-1α (25) data set. (Nodes that collapse in the strict consensus are marked with a black dot and do not alter the character mapping.) Third position sites in COI were excluded (downweighting yielded the same overall tree topologies) because this data partition showed a highly skewed base composition (91% A/T), significant base compositional heterogeneity among taxa (P ≤ 0.001), and an 8-fold higher rate of substitution than any of the other six data partitions. The total data set included 2,734 aligned nucleotide sites (2,321 with COI nucleotide 3 excluded; 394 parsimony informative sites). Trees were 1,765 steps in length and the consistency index was 0.3669. The tree was rooted by using five species of Lasioglossum s.s. The tree recovers several of the recognized subgenera of Lasioglossum (including Sphecodogastra and Dialictus) as well as many of the species groups of Evylaeus. Social behavior and parasitism (obtained from published studies listed in ref. 37) were mapped onto the tree by using macclade version 3.07 (27). Eusociality arose once in the common ancestor of the ingroup species excluding L. (“Dialictus”) figueresi. Reversals to either solitary nesting or social polymorphism (eusocial and solitary populations of the same species) occurred as many as five times. Social parasitism (in the subgenus Paralictus) is inferred to have arisen once. Methods are outlined in the text.

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