Variation in reproduction of the smallest‐bodied primate radiation, the mouse lemurs (Microcebus spp.): A synopsis

Abstract

Reproduction is a fundamental trait in the life history of any species and contributes to species diversity and evolution. Here, we aim to review the barely known variation in reproductive patterns of the smallest-bodied primate radiation, the Malagasy mouse lemurs, focusing on twelve species of four phylogenetic clades. We present a new reproductive field dataset collected between May and November 1996-2016 for nine species (Microcebus murinus, M. myoxinus, M. ravelobensis, M. bongolavensis, M. danfossi, M. sambiranensis, M. margothmarshae, M. mamiratra, and M. lehilahytsara) and add published field information on three additional species. In the majority of species, the estrus of females was recorded in the period of long days (day length longer than 12 hr), whereas male testes size increased about one to three months prior to this. Reproductive schedules varied considerably between the four clades. Sympatric species-pairs of different clades differed in the timing of female and male reproduction, suggesting strong phylogenetic constraints. Populations of the same species in a different ecological setting varied in the onset of reproduction, suggesting substantial environmental plasticity. Warm temperatures and rainfall throughout the year may allow for less expressed reproductive seasonality. Our results suggest that an interplay between phylogenetic relatedness, ambient temperature (as a proxy for thermo regulatory constraints), and rainfall (as a proxy for food availability), may best explain this variation. Findings further point to a more complex control of mouse lemur reproduction than previously described and illuminate phylogenetic constraints and adaptive potentials in behavioral reaction norms of a species-rich primate radiation.

Ecology and morphology of mouse lemurs (Microcebusspp.) in a hotspot of microendemism in northeastern Madagascar, with the description of a new species

“…Differences in reproductive schedules among mouse lemur species depend on phylogenetic relatedness, although environmental parameters (i.e., rainfall and temperature) likely play a role in fine‐tuning reproductive function (Evasoa et al, 2018). Although photoperiod is generally considered the main trigger of reproductive physiological function in mouse lemurs and is a relatively good predictor of food availability in seasonal habitats, there is substantial variation in the timing and duration of reproduction within and across mouse lemur species, as evident in our study populations.…”

“…Mouse lemurs are seasonal breeders and can already reproduce during their first year of life (Evasoa et al, 2018; Kraus, Eberle, & Kappeler, 2008; Schmelting, Zimmermann, Berke, Bruford, & Radespiel, 2007). Reproductive states were assessed using several morphological indicators (i.e., vaginal morphology and testis size) frequently used in the literature (e.g., Blanco, 2008; Randrianambinina, Rakotondravony, Radespiel, & Zimmermann, 2003; Wrogemann & Zimmermann, 2001).…”

“…The reproductive state of females was defined as anestrous (closed vagina, nonreproductive), pre‐estrous (swollen vagina), estrous (open vagina), pregnant (enlarged belly), or lactating (palpable and enlarged nipples that release milk under soft pressure). Male reproduction was assessed based on testes state: while being completely regressed in the nonbreeding season, testes increase considerably in size starting about 1–3 months before female estrus (Evasoa et al, 2018). However, testes size was measured slightly differently across our data set (i.e., left and right testes separately or only total width) and measures may also differ slightly between different researchers.…”

“…Besides using molecular data, species delimitation under an integrative taxonomic approach (e.g., Padial, Miralles, De la Riva & Vences, 2010) requires incorporating morphological and ecological information. While phenotypic differences between lineages could, for instance, indicate dietary preferences (e.g., Viguier, 2004), environmental and reproductive data can help to understand the role of habitat selection (Dammhahn & Kappeler, 2008; Rakotondravony & Radespiel, 2009) and reproductive schedules (Evasoa et al, 2018) during speciation.…”

An empirical estimate of the generation time of mouse lemurs

“…A major constraint for mouse lemur demographic research is that age determination is notoriously difficult. In general, mouse lemurs are seasonal breeders with infants being born during the rainy season (Rina Evasoa et al, ; Schmelting, Ehresmann, Lutermann, Randrianambinina, & Zimmermann, ). Surviving offspring can already reproduce in the subsequent mating season that starts toward the end of the next dry season (Kraus et al, , Schmelting et al, ; Zohdy et al, ).…”