Harmonizing hybridization dissonance in conservation

Abstract

A dramatic increase in the hybridization between historically allopatric species has been induced by human activities. However, the notion of hybridization seems to lack consistency in two respects. On the one hand, it is inconsistent with the biological species concept, which does not allow for interbreeding between species, and on the other hand, it is considered either as an evolutionary process leading to the emergence of new biodiversity or as a cause of biodiversity loss, with conservation implications. In the first case, we argue that conservation biology should avoid the discussion around the species concept and delimit priorities of conservation units based on the impact on biodiversity if taxa are lost. In the second case, we show that this is not a paradox but an intrinsic property of hybridization, which should be considered in conservation programmes. We propose a novel view of conservation guidelines, in which human-induced hybridization may also be a tool to enhance the likelihood of adaptation to changing environmental conditions or to increase the genetic diversity of taxa affected by inbreeding depression. The conservation guidelines presented here represent a guide for the development of programmes aimed at protecting biodiversity as a dynamic evolutionary system.

Fig. 1. Expected pattern of introgression of neutral genes between local and invasive organisms in range expansion.

a The context of this expected pattern of introgression is the expansion of an invasive species (in beige) in an area where the local species (in blue) is already in demographic equilibrium. The invasive species starts its colonization from the bottom left side of the area with few individuals. b The level of introgression is asymmetrical and higher in the invasive organisms when the interbreeding rate is large enough (after the dotted line in the x-axis). The value of the admixture rate that delineates this expected higher introgression in the invasive taxon depends on the combination of demographic and migration parameters. The introgression asymmetry between the two species is due to local alleles continuously introduced at the wave front of the invasive range expansion, with a relatively high probability of increasing in frequency due to the surfing process. The invasive organisms are not necessarily non-indigenous and may also represent threatened organisms that increase in frequency at the expense of exotic organisms.

Fig. 2. Three types of hybridization regarding the reproductive characteristics of first-generation hybrids (F₁).

Type 1 represents infertile or inviable hybrids. Type 2 hybrids are fertile but introgression is prevented in further generations due to the generation of gametes without recombination during gametogenesis in hybrid offspring. Type 3 hybrids are fertile and there is recombination during gametogenesis allowing introgression in further generations. Non-human-induced hybridization represents hybrids naturally found in nature, in which evolutionary opportunities arise when hybrids are fertile. Conservation guidelines are proposed for human-induced hybridization, which are motivated by any anthropogenic factor. They represent either a purely demographic or both a demographic and genetic effect on interbreeding taxa. The conservation priorities to avoid biodiversity loss are highlighted in red and basically represent human-induced hybridization that produces demographic decline or ecological disequilibrium. A potential tool to increase genetic diversity is highlighted in green.

Fig. 3. Identification of the type of hybridization.

Different steps that may be considered to recognize the type of hybridization when there is evidence of interbreeding between taxa (modified from Quilodrán et al.).