Environmental Conditions Affect the Magnitude of Inbreeding Depression in Survival of Darwin's Finches

Abstract

Abstract. Understanding the fitness consequences of inbreeding (inbreeding depression) is of importance to evolutionary and conservation biology. There is ample evidence for inbreeding depression in captivity, and data from wild populations are accumulating. However, we still lack a good quantitative understanding of inbreeding depression and what influences its magnitude in natural populations. Specifically, the relationship between the magnitude of inbreeding depression and environmental severity is unclear. We quantified inbreeding depression in survival and reproduction in populations of cactus finches (Geospiza scandens) and medium ground finches (Geospiza fortis) living on Isla Daphne Major in the Galápagos Archipelago. Our analyses showed that inbreeding strongly reduced the recruitment probability (probability of breeding given that an adult is alive) in both species. Additionally, in G. scandens, first-year survival of an offspring with f ϭ 0.25 was reduced by 21% and adults with f ϭ 0.25 experienced a 45% reduction in their annual probability of survival. The magnitude of inbreeding depression in both adult and juvenile survival of this species was strongly modified by two environmental conditions, food availability and number of competitors. In juveniles, inbreeding depression was only present in years with low food availability, and in adults inbreeding depression was five times more severe in years with low food availability and large population sizes. The combination of relatively severe inbreeding depression in survival and the reduced recruitment probability led to the fact that very few inbred G. scandens ever succeeded in breeding. Other than recruitment probability, no other trait showed evidence of inbreeding depression in G. fortis, probably for two reasons: a relatively high rate of extrapair paternity (20%), which may lead to an underestimate of the apparent inbreeding depression, and low sample sizes of highly inbred G. fortis, which leads to low statistical power. Using data from juvenile survival, we estimated the number of lethal equivalents carried by G. scandens, G. fortis, and another congener, G. magnirostris. These results suggest that substantial inbreeding depression can exist in insular populations of birds, and that the magnitude of the inbreeding depression is a function of environmental conditions.

The strength of the association between heterozygosity and probability of interannual local recruitment increases with environmental harshness in blue tits

“…This result is in agreement with that reported by Keller et al. (2002) in song sparrows ( Melospiza melodia ) as they found that inbred males produced fewer offspring in cooler years, but their productivity was similar in comparison with their outbred contemporaries after warm springs. Further, we have previously found that immigrant females, which represent the bulk of gene flow in blue tits, tend to be more heterozygous than residents in our study populations (García‐Navas, Ferrer, Sanz et al., 2014).…”

“…Here, we quantified the relationship between heterozygosity and fitness along an environmental continuum, comprising harsh (wet–cool) and benign (dry–warm) years. Our results suggest that interannual variability in environmental harshness can affect the magnitude of HFC (Forcada & Hoffman, 2014; Keller et al., 2002). Among the studied environmental parameters, only accumulated rainfall was associated with selection differentials for heterozygosity (Figure 3).…”

“…Inbreeding and reduced levels of genetic diversity have been found to negatively impact different components of fitness, including reproductive performance (Ortego et al., 2009; Seddon, Amos, Mulder, & Tobias, 2004), resistance to parasites (Acevedo‐Whitehouse et al., 2006; Hawley, Sydenstricker, Kollias, & Dhondt, 2005), and survival (Keller, Grant, Grant, & Petren, 2002; Olano‐Marin, Mueller, & Kempenaers, 2011a). The positive association between individual genetic diversity and fitness‐related traits arises when homozygotes are less fit than heterozygotes due to either heterozygote advantage (i.e., overdominance) or recessivity of deleterious or partly deleterious alleles (Charlesworth & Charlesworth, 1987; Keller & Waller, 2002).…”

Males with high genetic similarity to females sire more offspring in sperm competition in Peron's tree frogLitoria peronii

“…Inbreeding depression in the wild was largely believed to be non-existent for a long time, but has recently been repeatedly verified (reviewed in Frankham 1995Frankham , 2005, for example, in adder snakes Vipera berus (Madsen et al 1999) and Darwin's finches Geospiza sp. (Keller et al 2002), in the latter case only under nutritional constraints.…”

Seasonal stress drives predictable changes in inbreeding depression in field-tested captive populations of Drosophila melanogaster

“…Among the studies reviewed by Armbruster & Reed [9] only 9 of 34 measured inbreeding depression under field conditions and only 4 measured natural temporal variation in levels of inbreeding depression in wild populations [18 -21]. For example, in populations of Darwin's finches inbreeding depression for adult and juvenile survival was found to be strongly influenced by food availability and the presence of competitors [19], while in song sparrows periods of rain were shown to significantly increase inbreeding depression for hatching success [20]. However, none of the studies were able to quantify the level of stress.…”