Leucism in Akodon affinis (Allen, 1912) (Rodentia: Cricetidae)

Leucism is a condition where animals show loss of pigmentation on certain parts of the skin, without affecting soft tissue (Buckley 1982). In mammals, pigmentation results from the synthesis and distribution of melanin (Hearing and Tsukamoto 1991), which depends on several enzymatic factors that modulate pigmentation, especially tyrosinase (Hearing and Tsukamoto 1991; Oetting et al. 2003). Melanin plays important roles, including protective coloration, communication, sexual selection, absorption of free radicals and body protection from ionizing radiation (Levine and Krupa 1966; Hearing and Tsukamoto 1991; Caro 2005; Camargo et al. 2014). Leucism has been observed in small mammals such as bats (Velandia-Perilla et al. 2013) and rodents (Oliveira 2009; Camargo et al. 2014; Brito and Valdivieso-Berneo 2016). However, in Neotropical rodents, this condition is barely known, and it has only been reported in a few species (reviewed by Brito and Valdivieso-Berneo 2016).

The Colombian grass mouse, Akodon affinis (Allen 1912) (Cricetidae), is a medium-sized Neotropical rodent characterized by uniform dusky brown upper parts with yellowish hair tips, giving an overall olivaceous effect, and dark grayish brown venter with olivaceous hair tips (Pardiñas et al. 2015). This species is endemic from the Colombian Andes and is the only representative of the genus in this country (Pardiñas et al. 2015; Ramírez-Chaves et al. 2016). Considering the limited information on the population and natural history of this species (Pardiñas et al. 2015), our main goal was to report leucism in Akodon affinis for the first time, and its incidence in populations inhabiting different Andean mountain ranges.

A comprehensive examination of the Akodon affinis specimens deposited in the Mammals Collection of Universidad del Valle (UV), Colombia, was carried out. We recorded information on the incidence of traces of leucism for the 12 different localities where this species has been recorded. These localities were sampled across different years, mostly during fieldwork practices of Biology courses at UV, using 100 to 200 Sherman traps (200 in most cases, V. Rojas-Diaz pers. comm.). We used a two-tailed Fischer's exact test to explore the association between incidence of leucism and sex. For this analysis we only considered the localities (with all the individuals in each) where leucism was detected.

A total of 11 out of 96 (11.46 %) individuals were found to show traces of leucism in different parts of their body (Table 1, Appendix 1), including cheeks, dorsum and venter (Figure 1). The dorsum was the part where most individuals showed traces of leucism (n = 8), followed by cheeks (n = 5) and venter (n = 1). Some individuals presented more than one part of their body with traces of leucism. The analysis showed a significant association between sex and leucism (odds ratio = 8.965, P = 0.021), with males having a higher-than-expected incidence of leucism. Leucistic individuals were collected at five different localities (Appendix 1) from the Western and Central Andes of Colombia (Figure 2). The incidence of leucistic individuals per locality was high (Table 2), but fluctuated over time. There were more localities with leucistic individuals in the Central Andes than in the Western Andes (Figure 2).

Table 1
Traces of leucism in individuals of Akodon affinis (Allen, 1912) from Colombia.

Figure 1
Leucism in individuals of Akodon affinis from Colombia: A) Spots on the right cheek and next to the ear (UV 14,440). B) Spot on the dorsum (UV 13,343). C) Wide spot from dorsum to venter (UV 12,025). Photographs by L. Ruano.

Figure 2
Collection localities of Akodon affinis in the Colombian Andes. White and black triangles depict localities where individuals showed traces or no traces of leucism, respectively.

Table 2
Proportion of leucism observed in populations of Akodon affinis throughout the years.

This paper reports, for the first time, information on leucism in Akodon affinis populations and its incidence over time in several localities. Our results suggest that the presence of leucism in the sampled populations is as high as the incidence found for Akodon mollis in Cordillera de Chilla, Ecuador, a highly fragmented habitat (Brito and Valdivieso-Berneo 2016). The incidence of leucism in A. affinis is significantly associated with sex, and appears mainly on their dorsum and rostrum. However, there is insufficient information to assess the potential influence of leucism on survival (visibility to a predator) or reproduction (sexual selection).

It has been proposed that leucism can be the result of skin wounds in burrowing rodents of the Family Geomy-idae (S. T. Alvarez-Castaneda pers. com.). However, since leucism traits occur with different frequency in both sexes and with different prevalence in the localities we studied, we consider that leucism in A. affinis may be due to genetic factors.

Considering the effects of geographic isolation in the emergence of recessive traits (e. g., bottleneck effect; Bensch et al. 2000; Lopucki and Mróz 2010), our findings suggest that some populations of A. affinis might be experiencing inbreeding due to either the discontinuous distribution of this species (Roach 2016) or to habitat fragmentation in the Colombian Andes (Kattan et al. 1994; Kattan and Alvarez-López 1996). According to the International Union for Conservation of Nature (IUCN), A. affinis is listed as Least Concern since a large population is presumed from its wide overall distribution range (Roach 2016). Nevertheless, aside from its distribution, there is scarce information about the population ecology of this species (Pardiñas et al. 2015). Consequently, information on population dynamics and population genetics is needed to determine the conservation status of A. affinis.

We are grateful to all those people who over the years have been contributing to the growth and maintenance of the Mammals Collection of Universidad del Valle (UV); without their help, this work could not be possible. We also thank L. Ruano for taking the photographs. Finally, we thank S. T. Álvarez-Castañeda and two anonymous reviewers for their valuable comments. María Elena Sánchez-Salazar edited the English manuscript.