Genetic structure in a solitary rodent (Ctenomys talarum): implications for kinship and dispersal (original) (raw)

Abstract

The genetic structure of a population provides critical insights into patterns of kinship and dispersal. Although genetic evidence of kin structure has been obtained for multiple species of social vertebrates, this aspect of population biology has received considerably less attention among solitary taxa in which spatial and social relationships are unlikely to be influenced by kin selection. Nevertheless, significant kin structure may occur in solitary species, particularly if ecological or life history traits limit individual vagility. To explore relationships between genetic structure, kinship, and dispersal in a solitary vertebrate, we compared patterns of genetic variation in two demographically distinct populations of the talar tuco-tuco ( Ctenomys talarum ), a solitary species of subterranean rodent from Buenos Aires Province, Argentina. Based on previous field studies of C. talarum at Mar de Cobo (MC) and Necochea (NC), we predicted that natal dispersal in these populations is male biased, with dispersal distances for males and females being greater at NC. Analyses of 12 microsatellite loci revealed that in both populations, kin structure was more apparent among females than among males. Between populations, kinship and genetic substructure were more pronounced at MC. Thus, our findings were consistent with predicted patterns of dispersal for these animals. Collectively, these results indicate that populations of this solitary species are characterized by significant kin structure, suggesting that, even in the absence of sociality and kin selection, the spatial distributions and movements of individuals may significantly impact patterns of genetic diversity among conspecifics.

Figures (9)

ethanol until analysis. Upon completion of these proce- dures, the animal was released into the burrow system from which it had been captured. For animals caught in the focal sampling grids, the position at which each individual was captured was recorded to the nearest meter using a 10 x 10 m Cartesian coordinate system established at each grid at the start of trapping. Microsatellite analyses High molecular weight genomic DNA was extracted from tissue samples using the DNeasy Tissue Extraction Kit (QIAGEN, Inc.). Genetic variation was examined at 12 microsatellite loci that had been isolated from Ctenomys haigi (n = 5; Lacey et al. 1999) and Ctenomys sociabilis (n = 7; Lacey 2001). These loci were chosen for analysis due to their ability to produce well-resolved polymerase chain reaction (PCR) products for C. talarum; variability at these oci was not assessed prior to generating the data used in this study. PCR amplification conditions were those given by Lacey (2001). Fluorescently labelled PCR products were electrophoresed on 4% denaturing polyacrylamide gels on an ABI 377 automated sequencer (Applied Biosystems, nc.). A TAMRA GS350 size standard was run in all sample

ethanol until analysis. Upon completion of these proce- dures, the animal was released into the burrow system from which it had been captured. For animals caught in the focal sampling grids, the position at which each individual was captured was recorded to the nearest meter using a 10 x 10 m Cartesian coordinate system established at each grid at the start of trapping. Microsatellite analyses High molecular weight genomic DNA was extracted from tissue samples using the DNeasy Tissue Extraction Kit (QIAGEN, Inc.). Genetic variation was examined at 12 microsatellite loci that had been isolated from Ctenomys haigi (n = 5; Lacey et al. 1999) and Ctenomys sociabilis (n = 7; Lacey 2001). These loci were chosen for analysis due to their ability to produce well-resolved polymerase chain reaction (PCR) products for C. talarum; variability at these oci was not assessed prior to generating the data used in this study. PCR amplification conditions were those given by Lacey (2001). Fluorescently labelled PCR products were electrophoresed on 4% denaturing polyacrylamide gels on an ABI 377 automated sequencer (Applied Biosystems, nc.). A TAMRA GS350 size standard was run in all sample

Table 1 Sample sizes for analyses of spatial and genetic structure in Ctenomys talarum The number of adult females and males captured at Mar de Cobo (MC) and Necochea (NC) are indicated. Two sampling grids were established at each focal sampling locality; each grid contained 2-4 distinct clusters of burrows, as determined using sap1z. Hence, in each line of the table, the sum of adults captured in all clusters equals the sample size for the associated grid (except for one female in MC that did not belong to any of the identified clusters) and the sum of adults captured in both grids equals the sample size for the associated focal sampling locality.

Table 1 Sample sizes for analyses of spatial and genetic structure in Ctenomys talarum The number of adult females and males captured at Mar de Cobo (MC) and Necochea (NC) are indicated. Two sampling grids were established at each focal sampling locality; each grid contained 2-4 distinct clusters of burrows, as determined using sap1z. Hence, in each line of the table, the sum of adults captured in all clusters equals the sample size for the associated grid (except for one female in MC that did not belong to any of the identified clusters) and the sum of adults captured in both grids equals the sample size for the associated focal sampling locality.

Table 2 Mean nearest-neighbour distances (m) for animals captured within the same sampling grid at Mar de Cobo (MC) or Necochea (NC). Distances for all pairs of animals of a given sex composition are shown, as are distances for the subset of those pairs consisting of close kin (r 2 0.25). Data are presented as mean (+ 1 SD) distances; sample sizes (number of minimum distances computed) are given below each mean

Table 2 Mean nearest-neighbour distances (m) for animals captured within the same sampling grid at Mar de Cobo (MC) or Necochea (NC). Distances for all pairs of animals of a given sex composition are shown, as are distances for the subset of those pairs consisting of close kin (r 2 0.25). Data are presented as mean (+ 1 SD) distances; sample sizes (number of minimum distances computed) are given below each mean

Table 3 Mean (4 1 SD) pairwise r values for animals captured at Mar de Cobo (MC) and Necochea (NC) Estimates of r were generated for animals captured within (a) the same cluster of burrows and (b) the same trapping grid. Asterisks denote means that fall outside of 95% confidence intervals generated by Monte Carlo randomizations (100 iterations) of pairs of the same sex composition that were captured within (a) the same sampling grid or (b) the same study population. Values are presented as mean (+ 1 SD).

Table 3 Mean (4 1 SD) pairwise r values for animals captured at Mar de Cobo (MC) and Necochea (NC) Estimates of r were generated for animals captured within (a) the same cluster of burrows and (b) the same trapping grid. Asterisks denote means that fall outside of 95% confidence intervals generated by Monte Carlo randomizations (100 iterations) of pairs of the same sex composition that were captured within (a) the same sampling grid or (b) the same study population. Values are presented as mean (+ 1 SD).

Fig. 2 Percentage of pairs of individuals identified as close kin (r 2 0.25) at Mar de Cobo (MC) and Necochea (NC). The total number of pairs from which each percentage was calculated is indicated inside each bar. Different letters indicate statistically significant differences between percentages (2-way ANovA, Tukey P < 0.05). In (a), the percentage of pairs of close kin within clusters of burrows is shown. In (b), the percentage of pairs of close kin within focal sampling grids is shown.

Fig. 2 Percentage of pairs of individuals identified as close kin (r 2 0.25) at Mar de Cobo (MC) and Necochea (NC). The total number of pairs from which each percentage was calculated is indicated inside each bar. Different letters indicate statistically significant differences between percentages (2-way ANovA, Tukey P < 0.05). In (a), the percentage of pairs of close kin within clusters of burrows is shown. In (b), the percentage of pairs of close kin within focal sampling grids is shown.

Table 4 F,, values calculated for animals from Mar de Cobo (MC) and Necochea (NC). The spatial scales across which F,; was calculated are indicated Asterisks denote F,, values that are significantly different from zero. Sample sizes are given in parentheses.

Table 4 F,, values calculated for animals from Mar de Cobo (MC) and Necochea (NC). The spatial scales across which F,; was calculated are indicated Asterisks denote F,, values that are significantly different from zero. Sample sizes are given in parentheses.

Table 5 F,, values calculated for animals from Mar de Cobo (MC) and Necochea (NC). The spatial scales at which F,, was calculated are indicated Asterisks denote F,, values that are significantly different from zero. Sample sizes are given in parentheses

Table 5 F,, values calculated for animals from Mar de Cobo (MC) and Necochea (NC). The spatial scales at which F,, was calculated are indicated Asterisks denote F,, values that are significantly different from zero. Sample sizes are given in parentheses

Table 6 Amova results for all individuals from Mar de Cobo (MC) and Necochea (NC) The percentage column indicates the amount of total variance explained by each hierarchical spatial scale. P values were obtained by comparisons of observed values with those generated by random permutation in ARLEQUIN 2.000. d.f. represents the degrees of freedom in each analysis. ®-statistics are analogous to Wright's F-statistics and identify the correlation among alleles at each of the hierarchical levels.

Table 6 Amova results for all individuals from Mar de Cobo (MC) and Necochea (NC) The percentage column indicates the amount of total variance explained by each hierarchical spatial scale. P values were obtained by comparisons of observed values with those generated by random permutation in ARLEQUIN 2.000. d.f. represents the degrees of freedom in each analysis. ®-statistics are analogous to Wright's F-statistics and identify the correlation among alleles at each of the hierarchical levels.

Table 7 amova results for adults from Mar de Cobo (MC) and Necochea (NC) partitioned by sex The percentage column indicates the amount of total variance explained by each hierarchical spatial scale. P values were obtained by comparisons of observed values with those generated by random permutation in ARLEQUIN 2.000. d.f. represents the degrees of freedom in each analysis. ®-statistics are analogous to Wright's F-statistics and identify the correlation among alleles at each of the hierarchical levels.

Table 7 amova results for adults from Mar de Cobo (MC) and Necochea (NC) partitioned by sex The percentage column indicates the amount of total variance explained by each hierarchical spatial scale. P values were obtained by comparisons of observed values with those generated by random permutation in ARLEQUIN 2.000. d.f. represents the degrees of freedom in each analysis. ®-statistics are analogous to Wright's F-statistics and identify the correlation among alleles at each of the hierarchical levels.

Key takeaways

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  1. Significant kin structure exists in solitary Ctenomys talarum populations, influencing genetic diversity patterns.
  2. Female kin structure is more pronounced than male kin structure in both studied populations.
  3. Gene flow varies significantly between Mar de Cobo (MC) and Necochea (NC), affecting genetic substructure.
  4. Analyses reveal a male-biased natal dispersal pattern, with males dispersing further than females.
  5. The study predicts that ecological and life history traits limit individual vagility, affecting kinship and dispersal.

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