Many mammalian species use photoperiod as a predictive cue to time
seasonal reproduction. In addition, metabolic effects on the
reproductive axis may also influence seasonal timing, especially in
female small, short-lived mammals. To get a better understanding of how
annual cycling environmental cues impact reproductive function and
plasticity in small, short-lived herbivores with different geographic
origins, we investigated the mechanisms underlying integration of
temperature in the photoperiodic-axis regulating female reproduction in
a Northern vole species (tundra vole, Microtus oeconomus) and in
a Southern vole species (common vole, Microtus arvalis). We show
that photoperiod and temperature interact to determine appropriate
physiological responses; there is species-dependent annual variation in
the sensitivity to temperature for reproductive organ development. In
common voles, temperature can overrule photoperiodical spring-programmed
responses, with reproductive organ mass being higher at 10°C than at
21°C, whereas in autumn they are less sensitive to temperature. These
findings are in line with our census data, showing an earlier onset of
spring reproduction in cold springs, while reproductive offset in autumn
is synchronized to photoperiod. The reproductive organs of tundra voles
were relatively insensitive to temperature, whereas hypothalamic gene
expression was generally upregulated at 10°C. Thus, both vole species
use photoperiod, whereas only common voles use temperature as a cue to
control spring reproduction, which indicates species-specific
reproductive strategies. Due to global warming, spring reproduction in
common voles will be delayed, perhaps resulting in shorter breeding
seasons and thus declining populations, as observed throughout Europe.