Decoupled evolution of mating biology and social structure in Acromyrmex leaf-cutting ants

Abstract Insect societies vary greatly in their social structure, mating biology, and life history. Polygyny, the presence of multiple reproductive queens in a single colony, and polyandry, multiple mating by females, both increase the genetic variability in colonies of eusocial organisms, resulting in potential reproductive conflicts. The co-occurrence of polygyny and polyandry in a single species is rarely observed across eusocial insects, and these traits have been found to be negatively correlated in ants. Acromyrmex leaf-cutting ants are well-suited for investigating the evolution of complex mating strategies because both polygyny and polyandry co-occur in this genus. We used microsatellite markers and parentage inference in five South American Acromyrmex species to study how different selective pressures influence the evolution of polygyny and polyandry. We show that Acromyrmex species exhibit independent variation in mating biology and social structure, and polygyny and polyandry are not necessarily negatively correlated within genera. One species, Acromyrmex lobicornis, displays a significantly lower mating frequency compared to others, while another species, A. lundii, appears to have reverted to obligate monogyny. These variations appear to have a small impact on average intra-colonial relatedness, although the biological significance of such a small effect size is unclear. All species show significant reproductive skew between patrilines, but there was no significant difference in reproductive skew between any of the sampled species. We find that the evolution of social structure and mating biology appear to follow independent evolutionary trajectories in different species. Finally, we discuss the evolutionary implications that mating biology and social structure have on life history evolution in Acromyrmex leaf-cutting ants. Significance statement Many species of eusocial insects have colonies with multiple queens (polygyny), or queens mating with multiple males (polyandry). Both behaviors generate potentially beneficial genetic diversity in ant colonies as well as reproductive conflict. The co-occurrence of both polygyny and polyandry in a single species is only known from few ant species. Leaf-cutting ants have both multi-queen colonies and multiply mated queens, providing a well-suited system for studying the co-evolutionary dynamics between mating behavior and genetic diversity in colonies of eusocial insects. We used microsatellite markers to infer the socio-reproductive behavior in five South American leaf-cutter ant species. We found that variation in genetic diversity in colonies was directly associated with the mating frequencies of queens, but not with the number of queens in a colony. We suggest that multi-queen nesting and mating frequency evolve independently of one another, indicating that behavioral and ecological factors other than genetic diversity contribute to the evolution of complex mating behaviors in leaf-cutting ants.

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Breeding systems and genetic diversity in tropical carpenter ant colonies: different strategies for similar outcomes in Brazilian Cerrado savanna

Zoological Journal of the Linnean Society ◽

10.1093/zoolinnean/zlaa035 ◽

2020 ◽

Vol 190 (3) ◽

pp. 1020-1035 ◽

Cited By ~ 2

Author(s):

Marianne Azevedo-Silva ◽

Gustavo M Mori ◽

Carolina S Carvalho ◽

Marina C Côrtes ◽

Anete P Souza ◽

...

Keyword(s):

Genetic Diversity ◽

Genetic Relatedness ◽

Breeding Systems ◽

Mating Frequency ◽

Ant Colonies ◽

Eusocial Insects ◽

Low Genetic Diversity ◽

Carpenter Ant ◽

Cerrado Savanna ◽

The Impact

Abstract Eusocial insects tend to present low genetic diversity (GD) within colonies, which can increase with the co-occurrence of multiple queens (polygyny) or with multiple mating by a single queen (polyandry). Therefore, it is important to elucidate how these strategies influence GD, which in turn mediate population ecology and how organisms respond to their environment. We studied two carpenter ant species from the Brazilian savanna, Camponotus renggeri and C. rufipes. Using microsatellites, we evaluated the number of breeders, the genetic relatedness and the contribution of polygyny and polyandry to GD within colonies. Both species exhibited facultative polygyny. In C. renggeri, low related queens formed colonies jointly and present low mating frequency. In this species, colony GD increased with the number of queens. Contrastingly, closely related queens of C. rufipes formed polygynous colonies, exhibiting high mating frequency. In C. rufipes, both queens and males contributed to colony GD. Despite the differences, the two species have similar GD at the colony scale. Under low mating frequency, our data support that polygyny has evolutionary importance for increasing GD in ant colonies, a mechanism mainly conferred to polyandry. Although the impact of GD in variable ecological and adaptive contexts remains uncertain, this study highlights how distinct reproductive strategies may generate similar patterns of GD in ants.

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Genetic diversity analysis among pigeonpea genotypes adapted to South American regions based on microsatellite markers

Scientia Agricola ◽

10.1590/s0103-90162011000400007 ◽

2011 ◽

Vol 68 (4) ◽

pp. 431-439 ◽

Cited By ~ 3

Author(s):

Adna Cristina Barbosa de Sousa ◽

Rodolfo Godoy ◽

Danilo Augusto Sforça ◽

Tatiana de Campos ◽

Maria Imaculada Zucchi ◽

...

Keyword(s):

Genetic Diversity ◽

Microsatellite Markers ◽

Diversity Analysis ◽

South American ◽

Genetic Diversity Analysis

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Characterization of a New Set of Microsatellite Markers Suggests Polygyny and Polyandry in Atta cephalotes (Hymenoptera: Formicidae)

Journal of Economic Entomology ◽

10.1093/jee/toaa200 ◽

2020 ◽

Vol 113 (6) ◽

pp. 3021-3027

Author(s):

Vanessa Muñoz-Valencia ◽

Kirsi Kähkönen ◽

James Montoya-Lerma ◽

Fernando Díaz

Keyword(s):

Social Structure ◽

Microsatellite Markers ◽

Preliminary Analysis ◽

Null Alleles ◽

Atta Cephalotes ◽

Genetic Studies ◽

Leaf Cutting ◽

Polymorphic Microsatellite ◽

Population Viscosity

Abstract The leaf-cutting ant, Atta cephalotes L. (1758), is a major herbivore with great economic impact in the Neotropics. Because of its broad range and human-mediated dissemination, the ecology of this ant has received considerable attention; however, questions concerning its population genetics, dispersal, and social structure remain unexplored. Here, we aimed to identify and provide information on molecular and statistical performance of a suite of polymorphic microsatellite markers for A. cephalotes while demonstrating their utility for further genetic studies. We designed primer sequences targeting thousands of microsatellite loci and then screened 30 of these for amplification and polymorphism. Fifteen of these loci were selected and used to evaluate their polymorphism using 74 ants sampled from 15 different nests of the same location. This set of 15 loci exhibited variation of 2–20 alleles, with a mean heterozygosity of 0.57. All loci followed Hardy–Weinberg expectations with no evidence of linkage disequilibrium, while two loci showed evidence of null alleles. Our preliminary analysis suggested substantial nest differentiation with no population viscosity within the sampled location, as well as colonies with multiple queens (polygyny) and paternity (polyandry). Our newly identified microsatellites have proven to be highly informative to investigate gene flow, social structure and reproduction of this key agricultural pest.

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Genetic Diversity and Transferability of Rubus Microsatellite Markers to South American Rubus Species

The Molecular Basis of Plant Genetic Diversity ◽

10.5772/32838 ◽

2012 ◽

Author(s):

Marta L. ◽

Ana M. ◽

Marcela Uribe

Keyword(s):

Genetic Diversity ◽

Microsatellite Markers ◽

South American ◽

Rubus Species

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Recent demographic histories and genetic diversity across pinnipeds are shaped by anthropogenic interactions and mediated by ecology and life-history

10.1101/293894 ◽

2018 ◽

Cited By ~ 2

Author(s):

M.A. Stoffel ◽

E. Humble ◽

K. Acevedo-Whitehouse ◽

B.L. Chilvers ◽

B. Dickerson ◽

...

Keyword(s):

Genetic Diversity ◽

Life History ◽

Large Scale ◽

Biodiversity Loss ◽

Single Species ◽

Population Viability ◽

Breeding Habitat ◽

Comparative Approach ◽

Population Declines ◽

Effective Population

AbstractA central paradigm in conservation biology is that population bottlenecks reduce genetic diversity and negatively impact population viability and adaptive potential. In an era of unprecedented biodiversity loss and climate change, understanding both the determinants and consequences of bottlenecks in wild populations is therefore an increasingly important challenge. However, as most studies have focused on single species, the multitude of potential drivers and the consequences of bottlenecks remain elusive. Here, we used a comparative approach by integrating genetic data from over 11,000 individuals of 30 pinniped species with demographic, ecological and life history data to elucidate the consequences of large-scale commercial exploitation by 18th and 19th century sealers. We show that around one third of these species exhibit strong genetic signatures of recent population declines, with estimated bottleneck effective population sizes reflecting just a few tens of surviving individuals in the most extreme cases. Bottleneck strength was strongly associated with both breeding habitat and mating system variation, and together with global abundance explained a large proportion of the variation in genetic diversity across species. Overall, there was no relationship between bottleneck intensity and IUCN status, although three of the four most heavily bottlenecked species are currently endangered. Our study reveals an unforeseen interplay between anthropogenic exploitation, ecology, life history and demographic declines, sheds new light on the determinants of genetic diversity, and is consistent with the notion that both genetic and demographic factors influence population viability.

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Paternity in eusocial Hymenoptera

Philosophical Transactions of the Royal Society B Biological Sciences ◽

10.1098/rstb.1996.0087 ◽

1996 ◽

Vol 351 (1342) ◽

pp. 947-975 ◽

Cited By ~ 293

Keyword(s):

Genetic Diversity ◽

Multiple Paternity ◽

Significant Negative Correlation ◽

Female Offspring ◽

Egg Laying ◽

Future Research ◽

Mating Frequency ◽

Eusocial Insects ◽

Helping Behaviour ◽

Using Data

Variation in paternity frequency in colonies of eusocial insects has profound effects on the relatedness among offspring and on the genetic diversity of colonies. Data on queen ‘mating-frequency’ in eusocial Hymenoptera vary in both quality and the phase of the ‘mating’ process they address. Some are observational studies of the range or maximum number of copulations; others are derived from estimates of the number of sperm in males and queens; others use genetic techniques to determine the paternity of different males among female offspring. Only the latter data can be used to calculate relatedness among offspring females. Previous reviews drew attention to these problems, but their results have established the impression that high paternity frequencies are common, largely because multiple copulations are frequently observed. For ants, we show that: (i) the range of observed copulations overestimates effective paternity frequency; and (ii) the mean effective paternity frequency in 19 species, for which accurate data based on allozyme analysis of mother — offspring combinations are available, is only 1.16 (range 1-1.48). Over one third of these species have queens in which only one male contributes to paternity. Data from 34 species, which include less detailed genetic studies and four species studied using sperm counts, give similar results. Only two species, both Atta leaf cutter ants and both studied using data on sperm stored in queen spermathecas, appear to have effective insemination frequencies above two. Data on bees and wasps show a similar trend. We conclude that reliably documented high paternity or insemination frequencies (> 2) are currently restricted to one phylogenetically isolated and highly eusocial taxon each in ants, eusocial bees and wasps ( Atta, Apis and Vespula , respectively). This pattern justifies the working hypothesis that multiple mating, by lowering the relatedness between female offspring and thereby the benefits of reproductive helping behaviour, has not been a general constraint for the evolution of eusociality in the Hymenoptera. Using reliable data on paternity frequency and insemination, we re-analyse two factors that it has been suggested correlate with mating frequency: colony population and number of egg-laying queens per colony. We find the following. 1. There is a significant positive correlation between paternity/insemination frequency and colony size for monogynous ants, but not for polygynous ants. This result seems to support the ‘sperm limitation’ hypothesis, that queens which need to be highly fecund copulate multiply to store sufficient sperm. We note, however, that the same trend is expected when large and/or long-lived colonies profit more from having genetically diverse offspring. 2. There is no significant negative correlation between paternity/insemination frequency and number of queens per colony. However, when the analysis is restricted to species with large colonies and no intranidal mating, the correlation between paternity frequency and queen number becomes marginally significant. Several previous reviews have addressed the possible adaptive significance of multiple paternity. In contrast, and in keeping with the data that show single paternity to be frequent, we discuss selective reasons for single or low paternity. We compare the relative effects of multiple paternity and multiple maternity on genetic diversity within colonies and show that they are not equivalent, and we also discuss directions for future research on paternity issues in social insects.

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