Anthropogenic disturbance and evolutionary parameters: a lemon shark population experiencing habitat loss

Abstract

The level of genetic variation in natural populations influences evolutionary potential, and may therefore influence responses to selection in the face of future environmental changes. By combining long-term monitoring of marked individuals with genetic pedigree reconstruction, we assessed whether habitat loss influenced genetic variation in a lemon shark (Negaprion brevirostris) population at an isolated nursery lagoon (Bimini, Bahamas). We also tracked changes in the strength and direction of natural selection. Contrary to initial expectations, we found that after the habitat loss neutral genetic variation increased, as did additive genetic variance for juvenile morphological traits (body length and mass). We hypothesize that these effects might result from philopatric behavior in females coupled with a possible influx of male genotypes from other nursery sites. We also found changes in the strength of selection on morphological traits, which weakened considerably after the disturbance; habitat loss therefore changed the phenotypes favored by natural selection. Because such human-induced shifts in the adaptive landscape may be common, we suggest that conservation biologists should not simply focus on neutral genetic variation per se, but also on assessing and preserving evolutionary parameters, such as additive genetic variation and selection.

Keywords: additive genetic variance; evolutionary potential; heritability; heterozygosity; human disturbance; selection.

Figure 1

Aerial photograph of the North Sound at Bimini, Bahamas, in 1980 (A), and again after resort development in 2003 (B; Photo credits: S. Kessel).

Figure 2

Aerial photograph of the North Sound at Bimini, Bahamas in 2003 (A), and this same area after further mangrove removal in 2005 (B; Photo credits: S. Kessel).

Figure 3

The proportion of age-0 lemon sharks not surviving their first year (black circles), or age-1 lemon sharks not surviving to age-2 (open circles), from 1995 to 2005. The black arrow indicates the approximate onset of disturbance on the x-axis. Values are means ± 1 SEM.

Figure 4

Number of reproducing males (A) and females (B) using the Bimini nursery site each year from 1995 to 2007. It should be noted that the majority of these individuals (92% of females and 99% of males) were genetically inferred and never physically captured. The black arrow indicates the approximate onset of disturbance on the x-axis.

Figure 5

Mean allelic richness (A) and expected heterozygosity (B) for juvenile lemon sharks captured at Bimini, Bahamas from 1995 to 2007 (n = 1131). Values are means ± 1 SEM. The black arrow indicates the approximate onset of disturbance on the x-axis.

Figure 6

Linear (directional) selection coefficients acting on the length (A,B), mass (E), and growth rate (C,D) of newborn (i.e., age-0) and age-1 juvenile lemon sharks. Values are means ± 1 SEM. The black arrow indicates the approximate onset of disturbance on the x-axis.

Figure 7

Relationship between initial precaudal length (A,B), body mass (C,D), or growth rate (E) and an individual's absolute fitness for each cohort of age-0 (A,C) and age-1 (B,D,E) juvenile lemon sharks. The lines are univariate cubic splines (see Schluter 1988). Growth was calculated for the interval preceding that (i.e., age-0 to age-1) over which selection was estimated (i.e., age-1 to age-2) and thus only available for age-1 juveniles.